Abstract The emergence of Arabidopsis as a model species and the availability of genetic and genomic resources have resulted in the identification and detailed characterization of abiotic stress signalling pathways. However, this has led only to limited success in engineering abiotic stress tolerance in crops. This is because there needs to be a deeper understanding of how to combine resistances to a range of stresses with growth and productivity. The natural variation and genomic resources of Arabidopsis thaliana (Arabidopsis) are a great asset to understand the mechanisms of multiple stress tolerances. One natural variant in Arabidopsis is the accession C24, and here we provide an overview of the increasing research interest in this accession. C24 is highlighted as a source of tolerance for multiple abiotic and biotic stresses, and a key accession to understand the basis of basal immunity to infection, high water use efficiency, and water productivity. Multiple biochemical, physiological, and phenological mechanisms have been attributed to these traits in C24, and none of them constrains productivity. Based on the uniqueness of C24, we postulate that the use of variation derived from natural selection in undomesticated species provides opportunities to better understand how complex environmental stress tolerances and resource use efficiency are co-ordinated. Abiotic stress, accession C24, Arabidopsis, defence, growth, trade-off Introduction The early evolution of land plants took place in dry conditions and under greatly fluctuating temperatures (Bateman et al., 1998; Beerling et al., 2001). Conversely, the domestication of crop plants occurred later under relatively stress-free environmental conditions, leading to dramatic phenotypic changes with the primary aim to maximize yield (Hancock, 2005; Gepts, 2010; Meyer et al., 2012). Life history theory has long proposed that organisms differ as a result of how they resolve competing demands on their resources, particularly between growth and other functions (Koricheva et al., 2004). Although agricultural breeding aims to combine high yields with other important investments such as abiotic and biotic stress resistance, some of these investments may trade-off against one another, preventing maximum allocation to all functions (Anderson, 2016). In this context, crop domestication under artificially benign environments could be viewed as one extreme ‘trade-off’, where growth investments have been enhanced at the expense of stress resistance, crop management being a substitute for the need to maintain a full panel of stress-resistant phenotypes. Consequently, the selection for productivity traits has not always resulted in plants that maintain productivity when subjected to abiotic or biotic stress (Herms and Mattson, 1992; Heil, 2014). As sessile organisms, plants are dependent on defence mechanisms in their response to abiotic challenges that impact upon growth and productivity. Therefore, abiotic stresses not only constrain the ecological limits of natural species (Normand et al., 2009) but also contribute towards reduced agricultural productivity (Mittler, 2006; López-Arredondo et al., 2015). Climate change will continue to increase the incidences and detrimental effects of abiotic stresses on plant growth and productivity, and it will probably further contract agricultural land area (Holman et al., 2017) and range limits (Guisan and Thuiller, 2005; Normand et al., 2009). Furthermore, abiotic stress may negatively influence the occurrence and spread of pathogens, insects, and weeds (Compant et al., 2010; Pautasso et al., 2012; Peters et al., 2014; Anderegg et al., 2015). Therefore, it is imperative that we understand how plant growth, survival, and pathogen incidences are balanced in the face of abiotic stress. As an undomesticated species that has been subject to a complex suite of environmental challenges over the course of its evolutionary history, Arabidopsis (Arabidopsis thaliana) has the potential to help us understand the viability of combining tolerance to multiple stresses, whilst at the same time fine-tuning the balance between defence, growth, and productivity. We therefore briefly review the current understanding of the interplay between abiotic stress tolerance and plant growth, and then focus on the accession C24 as a potential model genotype for future research into enhancing multiple stress tolerances and resource use efficiency. Plant growth responses under abiotic stress Already in the early 1980s it was noted that environmental factors limit crop production by as much as 70% (Boyer, 1982), and in 2007 a report by the FAO/IIASA highlighted that 96% of the global land area is affected by some form of severe environmental constraint (http://www.fao.org/docrep/010/a1075e/a1075e00.htm, last accessed December 2017). Plant responses to changes in the environment are highly complex and dynamic, involving global reprogramming of transcription, metabolism, and resource allocation in order to adapt to these changes. These responses and the concurrent adjustment of physiology and phenology have consequences for growth and productivity. For example, drought, salinity, and low temperature all impose osmotic stress that can lead to a reduction in turgor pressure (Chaves et al., 2009). As a consequence, membranes may become disordered (Yamamoto, 2016), proteins may be denatured, and oxidative damage may occur due to the production of excess reactive oxygen species (ROS; Galvez-Valdivieso and Mullineaux, 2010; Baxter et al., 2014; Petrov et al., 2015). When taking the general metabolic dysfunction and damage of many cellular structures into consideration, it is inevitable that environmental stress will limit growth and reproduction. Understanding the molecular reprogramming events that occur during abiotic stress has therefore been of great interest for many decades. Plant hormones such as abscisic acid (ABA), gibberellin (GA), jasmonic acid (JA), salicylic acid (SA), and ethylene (ET) play an important role in integrating plant growth and development with biotic and abiotic stress responses (Vlot et al., 2009; Zhu et al., 2011; Verma et al., 2016). While SA, JA, and ET preferentially mediate the defence responses against pathogens and pests (Liu et al., 2008), ABA is more typically known for defence against abiotic stresses (Raghavendra et al., 2010; Cramer et al., 2011; Sah et al., 2016). However, it is evident that hormones do not function in discrete pathways, but rather influence each other at different levels (i.e. biosynthesis or signalling) to control environmental and developmental signalling (Gray, 2004; Verma et al., 2016). The picture is further complicated by the fact that interactions can be either synergistic or antagonistic, and the outcome of modulating hormone levels often leads to contradictory results, where up-regulation of a given hormone is found to confer stress adaptation in one case, but impairs survival in a different case, depending on the intensity, nature, and timing of the stress (Raghavendra et al., 2010; Ye et al., 2012; Leng et al., 2014; Rejeb et al., 2014; Kazan, 2015; Souza et al., 2017). The complex interactions that co-ordinate growth and stress tolerance are subject to continual investigation and are far from being resolved. An in-depth evaluation of hormone functions and crosstalk under the many different stress conditions is beyond the scope of this review. Therefore, only a brief description of the major plant hormones and how they integrate plant growth with stress responses will be provided. ABA, SA, JA, ET, and GA regulate a wide range of developmental responses including embryo maturation, seed development, seed production, seed dormancy, seed germination, vegetative growth, flower formation, secondary metabolism, and senescence (Karssen et al., 1983; Pauwels et al., 2008; Pantin et al., 2013; Liu et al., 2015). ABA also controls many stress responses, functions as a key regulator in the adaptation to drought and salinity stress, and inhibits growth by triggering transcriptional changes in stress adaptation mechanisms, and carbohydrate and lipid metabolism (Umezawa et al., 2010; Fujita et al., 2011). In recent years, many excellent reviews have been dedicated to the subject of ABA perception and signalling pathways during plant development and stress responses (Cutler et al., 2010; Raghavendra et al., 2010; Santiago et al., 2012). In essence, ABA-responsive transcription factors, such as ABI5 and the AREB/ABF family, control many ABA-responsive genes integrating abiotic stress signals and plant developmental processes (Fujita et al., 2011, 2013); consequently, ABA sits at the interface between many plant stress responses and primary metabolism, highlighting its broad role in a variety of cellular responses (Hey et al., 2010; Muñoz-Bertomeu et al., 2011). Many reports of the role of SA and JA in abiotic stress signalling have also emerged in recent years (Clarke et al., 2004, 2009; Brossa et al., 2011; Wasternack and Hause, 2013; de Ollas et al., 2015). SA and JA biosynthesis is triggered by abiotic stresses, and both function as signalling molecules independently, or in connection with ABA, to regulate many physiological responses including stomatal conductance, photosynthesis, respiration, and antioxidant capacity associated with the protection against osmotic, drought, salt, heat, and UV stress signalling pathways (Horváth et al., 2007, 2015; Szepesi et al., 2009; Wang et al., 2010; Hou et al., 2010; Rivas-San Vicente and Plasencia, 2011; Boatwright and Pajerowska-Mukhtar, 2013; Khan et al., 2013; Miura and Tada, 2014; Muñoz-Espinoza et al., 2015). Extensive reviews on the role of SA and JA during abiotic stress have recently been published, which provide excellent overviews on both hormones and their interactions with ABA (Khan et al., 2015; Riemann et al., 2015). Plant growth is often severely reduced under abiotic stress conditions, and the plant growth-promoting hormone GA (Richards et al., 2001; Sun, 2010) may be involved in growth suppression under abiotic stress (Colebrook et al., 2014). Key components of the GA signalling pathway are the growth-repressing DELLA proteins (DELLAs; Peng et al., 1997; Alvey and Harberd, 2005; Feng et al., 2008), which are a subset of the GRAS family of transcriptional regulators (Zentella et al., 2007; Feng et al., 2008). First indications of an involvement of GA in plant stress responses came from early studies on growth retardants that inhibit GA biosynthesis, but also led to enhanced stress tolerance (Gilley and Fletcher, 1998; Rademacher, 2000). Specifically, JA, ET, and ABA signalling pathways are functionally modulated by GA, regulating both abiotic stress and developmental responses (Achard, 2006; Achard et al., 2007, 2008; Golldack et al., 2013; Liu et al., 2016). For example, the regulation of ABA biosynthesis in response to abiotic stress has been linked to GA signalling, where ABA production is increased through the DELLA target gene XERICO (Zentella et al., 2007; Ariizumi et al., 2013), and overexpression of XERICO in rice conferred drought and salt stress tolerance through ABA-mediated stress responses (Zeng et al., 2015). There are many more examples of the interaction and involvement of both ABA and GA signalling pathways in modulating plant growth in the face of abiotic stress, which has been extensively reviewed recently (Colebrook et al., 2014; Verslues, 2017). In addition, the transient accumulation of two DELLAs under low temperature inhibited root growth, which was linked to the cold-inducible transcription factor gene CBF1, a member of the AP2/ETHYLENE RESPONISVE ELEMENT BINDING PROTEIN family, resulting in cold acclimation and freezing tolerance (Achard et al., 2008). Similarly, the growth of Arabidopsis seedlings is inhibited under salt stress due to a DELLA-dependent mechanism utilizing the SERINE/THREONINE PROTEIN KINASE (CTR1)- and ETHYLENE INSENSTIVE 3 (EIN3)-dependent ET response pathway (Achard, 2006). This suggests that a DELLA-dependent growth restriction is advantageous to plants as it may permit a flexible modulation of growth in response to environmental stress. Importantly, several DELLA-interacting proteins have been shown to be components of other hormone signalling pathways, providing a mechanism for GA signalling to interact with these pathways (Gallego-Bartolome et al., 2012; Golldack et al., 2013; Hou et al., 2013). For example, growth and defence trade-offs also involve jasmonates, which act antagonistically to GA through proteasome-dependent degradation of the transcriptional repressors JASMONATE ZIM-DOMAIN (JAZ) and DELLAs. Specifically, jasmonates delay GA-mediated DELLA protein degradation, inhibiting growth during wounding and fungal pathogen infection (Hou et al., 2010; Kazan and Manners, 2011; Yang et al., 2012); however, recently an uncoupling between growth and defence through a relief of the transcription repression in a phytochrome B-dependent manner was observed, integrating light and defence signalling pathways (Campos et al., 2016; Cerrudo et al., 2017). In essence, plant responses are fine-tuned by a network of hormonal signalling cascades that constantly evaluate the need to grow with the need to defend, and balance resource allocation according to these requirements (Leone et al., 2014). However, the major paradigm of the growth–defence trade-offs in plant disease and pest resistance (Heil and Baldwin, 2002; Eichmann and Schäfer, 2015) has recently come under scrutiny for its rather one-dimensional view that allocation of limited metabolic resources to one process automatically reduces the energy allocation to other processes (Kliebenstein, 2016). Can we learn lessons from Arabidopsis? The evolutionary emergence of stress tolerance, and subsequent domestication of crop plants, implies that undomesticated plants species, which have not been shaped by breeding for particular traits, could be useful to identify novel potential for improving stress tolerance (Kant and Baldwin, 2007). In this context, Arabidopsis has played a critical role in unravelling abiotic stress signal transduction pathways. Since its introduction as a model plant species (Alonso-Blanco and Koornneef, 2000; Koornneef and Meinke, 2010), it has rapidly expanded our knowledge of abiotic stress signalling mechanisms, as evident by the many papers published during the last two decades (6112 papers; PubMed search terms: abiotic stress, drought-, heat-, salt-, ozone- or heavy metal stress, and Arabidopsis), with the greatest advance occurring within the last 5 years (3017 papers between 2012 and 2016; http://www.ncbi.nlm.nih.gov/pubmed, last accessed 6 February 2018; Fig. 1). This expansion in publications has been aided by the increased availability of powerful experimental and analytical tools, and by the generation and analysis of large data sets of plants subjected to single and/or combined abiotic stresses. This has led to the identification of many stress-inducible genes and gene regulatory networks, followed by the manipulation of gene expression in Arabidopsis (Kim et al., 2012; Hartmann et al., 2015; Yoshida et al., 2015; Bechtold et al., 2016). Fig. 1. View largeDownload slide PubMed search for publications using search terms: abiotic stress, or drought-, or heat-, or salt-, or ozone-, or heavy metal stress and Arabidopsis. Fig. 1. View largeDownload slide PubMed search for publications using search terms: abiotic stress, or drought-, or heat-, or salt-, or ozone-, or heavy metal stress and Arabidopsis. Over the past two decades, the Arabidopsis community has taken advantage of the vast genetic diversity present within this model species. The availability of genomic data and molecular tools in Arabidopsis is therefore an asset to natural variation-based studies and allows for the identification of polymorphisms responsible for phenotypic variation of single and multiple traits. Consequently, natural variation in conjunction with quantitative trait locus (QTL) mapping has frequently been used to identify genetic regions responsible for abiotic stress tolerance such as drought, ozone, and osmotic stress (Bouchabke et al., 2008; Lasky et al., 2014; Trontin et al., 2014; Xu et al., 2015), as well as growth and developmental processes under controlled and natural conditions (Barth et al., 2003; Lisec et al., 2008; Brachi et al., 2010; Meyer et al., 2010; Prinzenberg et al., 2010; Fujimoto et al., 2012). Many different quantitative genetic studies investigating responses to changes in the environment have led to the identification of loci and genetic regions involved in regulating plant development (McKay et al., 2003, 2008; Juenger et al., 2005; Bechtold et al., 2013, 2016, Bac-Molenaar et al., 2015a, b) and, given the overall impact abiotic stress has on physiology and growth, it is not unsurprising that development and stress tolerance QTLs regularly co-localize. The accession C24 combines abiotic and biotic stress resistance with minimal impact on growth Whereas transgenic-centric research has largely focused on a few very well-studied accessions, most notably Columbia (Col-0), other accessions, such as the Iberian (Portuguese) accession C24, have received considerably less attention. Nevertheless, C24 has been included as a reference accession in enough comparative studies to bring about the emergence of an interesting picture with respect to its genome structure, gene expression patterns, stress resilience, growth, and physiology. C24 seemingly combines many abiotic and biotic stress tolerances without apparent growth penalties, as discussed below. C24 has a moderate tolerance to elevated ozone (Brosché et al., 2010; Xu et al., 2015), which was linked to a low stomatal conductance phenotype compared with ozone-sensitive accessions (Brosché et al., 2010). The co-localization of ozone sensitivity and high-water loss QTLs in a Col-0×Cvi-0 recombinant inbred line (RIL) population supported this notion (Brosché et al., 2010). In addition, a functional relationship between stomatal responses and ozone sensitivity has been postulated for many other plants species including snap beans, grasses, deciduous trees, and soybean (Mills et al., 2009; Paoletti and Grulke, 2010; Hoshika et al., 2015; Osborne et al., 2016). However, further investigation of ozone tolerance in C24 using an additional mapping population (C24×Te RIL) suggested that elevated SA-mediated defences also facilitated ozone tolerance in C24 (Xu et al., 2015). SA-associated defences are normally induced in response to pathogen infection (Boatwright and Pajerowska-Mukhtar, 2013), yet it has long been known that ozone- and pathogen-induced defence responses share close similarities that are mediated via the SA signalling pathway (Kangasjärvi et al., 1994; Sandermann et al., 1998). Exposure of Arabidopsis to ozone or hydrogen peroxide (H2O2) initiates the biosynthesis of SA and hypersensitive cell death (Overmyer et al., 2005). In addition, SA has been directly linked to regulating stomatal aperture by inducing ROS production in guard cells in an SIZ1-dependent manner. SIZ1 negatively affects stomatal movement by repression of SA accumulation independent of ABA, and elevated SA levels in siz1 mutants lead to a reduced stomatal aperture, accumulation of ROS in the guard cells, and promotion of drought tolerance (Miura et al., 2013). Similarly, other SA-accumulating mutants such as acd6 and cpr5 also improved drought tolerance by preventing light-induced stomatal opening (Okuma et al., 2014). C24 has previously been shown to have elevated SA, H2O2, and glutathione levels, and constitutive expression of cell death- and stress-associated genes under non-stressful conditions (Bechtold et al., 2010; Fig. 2), similar to the Constitutive Expresser of PR1-6 (cpr6-1) mutant (Bechtold et al., 2010). Consequently, C24 is resistant to a number of pathogens, including Hyaloperonsopora arabidopsidis (Lapin et al., 2012), Pseudomonas syringae pv. tomato (Ton et al., 1999), Cucumber mosaic virus (Takahashi et al., 2002; Sekine et al., 2008), and Oidium neolycopersici (powdery mildew; Gao et al., 2015). While natural variation in different resistance genes, including the coiled-coil (CC)-NBS-LRR-type protein gene RCY1 (Takahashi et al., 2002), PATATIN-LIKE PROTEIN2 (PLP2; La Camera et al., 2005), and ENHANCED DISEASE RESISTANCE1 (EDS1; Gao et al., 2015), has been identified as the primary cause of some of the pathogen resistances, a significantly reduced transformation rate using a range of Agrobacterium tumefaciens strains via the floral dip method (Ghedira et al., 2013; Fig. 2) also points to a more general non-specific resistance mechanism. The reduced stomatal conductance in C24 may be of significance (Bechtold et al., 2010; Brosché et al., 2010; Fig. 2), as stomatal opening is an important component in plant innate immunity where stomatal aperture is regulated in response to bacterial invasions (Melotto et al., 2006; Zeng et al., 2010). Correspondingly, Agrobacterium transformation frequency using the floral dip method has also been connected to the state of stomatal opening (Chumakov et al., 2002). Interestingly, despite the already lowered stomatal conductance seen in a number of studies including our own, C24 also belongs to a group of five out of 40 accessions whose stomata are among the most sensitive to further closure stimuli, such as ABA, where ABA production in response to desiccation was inversely correlated to foliar ABA levels prior to stress (Aliniaeifard and Van Meeteren, 2014). This enhanced stomatal closure, which in C24 may be linked to the increased foliar SA levels (Bechtold et al., 2010; Miura et al., 2013; Okuma et al., 2014), could further contribute to the observed pathogen resistances. Fig. 2. View largeDownload slide Overview of stress tolerances and molecular changes in Arabidopsis accession C24. Orange boxes indicate stress tolerances and growth phenotypes observed in C24, the blue text indicates molecular and physiological changes observed in C24, and purple arrows connect potentially underlying molecular changes to the observed phenotypes. Constitutive R gene/defence gene expression includes PR-1, WRKY, MYB, RCY1, EDS1, and PLP2. Constitutive HEAT SHOCK TRANSCRIPTION FACTOR (HSF) and HEAT SHOCK PROTEIN (HSP) gene expression. Fig. 2. View largeDownload slide Overview of stress tolerances and molecular changes in Arabidopsis accession C24. Orange boxes indicate stress tolerances and growth phenotypes observed in C24, the blue text indicates molecular and physiological changes observed in C24, and purple arrows connect potentially underlying molecular changes to the observed phenotypes. Constitutive R gene/defence gene expression includes PR-1, WRKY, MYB, RCY1, EDS1, and PLP2. Constitutive HEAT SHOCK TRANSCRIPTION FACTOR (HSF) and HEAT SHOCK PROTEIN (HSP) gene expression. The overall low stomatal conductance, increased stomatal sensitivity to ABA, and elevated SA levels also integrate the observed abiotic stress tolerances, including a greater degree of rosette drought tolerance and reduced water use (Bechtold et al., 2010; Miura and Tada, 2014). Significant variation between Col-0, Ws-0, Ws-2, and C24 for absolute water use was observed over the entire life cycle of the plant (Bechtold et al., 2010), and correlated positively with daily water use (Fig. 3). This suggested that accessions increased water use in both the short and long term (Bechtold et al., 2010, 2013; Fig. 3), independent of flowering time. Furthermore, C24 demonstrated markedly reduced water use across both time frames compared with the other accessions. The mechanistic basis of the capacity of C24 to resist drought stress is interesting from the point of view of understanding adaptation to the environmental characteristics that are synonymous with its ecological niche (i.e. reduced water availability). However, its reduced water use is perhaps more interesting from an agronomic standpoint, especially since it is combinable with multiple abiotic stress resistances, without a reduction in productivity (Bechtold et al., 2010; Ferguson et al., 2018). Fig. 3. View largeDownload slide Relationship between daily water use and long-term water use in four accessions (Col-0, Ws-2, Ws-0, and C24) and two mutant lines (35S:AtHSFA1b in Ws-2 and Col-0 background, respectively) under well-watered (80% rSWC) and moderate drought (40% rSWC) conditions (Bechtold et al., 2010, 2013). The linear model of the relationship between mean long-term water use and mean daily water use is provided as the fit line. R2 and P-values are provided. Fig. 3. View largeDownload slide Relationship between daily water use and long-term water use in four accessions (Col-0, Ws-2, Ws-0, and C24) and two mutant lines (35S:AtHSFA1b in Ws-2 and Col-0 background, respectively) under well-watered (80% rSWC) and moderate drought (40% rSWC) conditions (Bechtold et al., 2010, 2013). The linear model of the relationship between mean long-term water use and mean daily water use is provided as the fit line. R2 and P-values are provided. Interestingly, C24 is also the most submergence tolerant amongst 84 accessions, exhibiting high root oxygen under light and dark conditions (Vashisht et al., 2011). While low stomatal conductance, high root oxygen levels, and lower leaf mass area may be beneficial for drought and submergence tolerance at the rosette stage (Mommer et al., 2007; Fig. 2), it is proposed that evolutionary selection has favoured leaf cooling over water conservation in Arabidopsis (Crawford et al., 2012) and, as such, this could have a negative impact on acclimation to elevated temperatures. Despite this, C24 seeds are tolerant to a 50 °C 1 h heat stress treatment, showing enhanced germination and seedling growth post-treatment compared with Col-0, Ler, Cvi, and Ws (Silva-Correia et al., 2014). However, it is not clear whether this heat tolerance phenotype translates to mature rosettes, as thermo-tolerance at the plant level involving C24 has been predominantly tested on plate-grown seedlings (Sanchez-Bermejo et al., 2015). From a physiological point of view, the lowered stomatal conductance and elevated leaf temperatures (Bechtold et al., 2010) in fully developed rosettes in C24 suggest a reduced capacity for evaporative cooling even under elevated air temperatures. In contrast to heat tolerance, C24 is more sensitive to osmotic stress, such as high salinity (Jha et al., 2010; Schmöckel et al., 2015) and freezing temperatures (Rohde et al., 2004; Hannah et al., 2006). Under salt stress, C24 exhibits reduced growth and increased shoot Na+ concentrations compared with tolerant Ws and Ler accessions (Jha et al., 2010). It appears that C24 is unable to respond to increases in salinity, as it fails to induce expression of key salt stress-responsive genes, namely VACUOLAR H(+)-PPase (AVP1) and NA+/H+ EXCHANGER 1 (NHX1) (Jha et al., 2010). Furthermore, it lacks the NaCl-specific component of the cytosolic calcium signature (Schmöckel et al., 2015), and it has been reported that C24 lacks an Na+ sensor, and therefore is unable to mount an appropriate response (Jha et al., 2010). However, the fact that C24 is highly drought tolerant (Bechtold et al., 2010) implies that the susceptibility to salt may not be due to a reduction in water availability during osmotic stress, but rather due to the toxicity of the accumulating Na+ cations. Under non-stressful conditions, transcriptional differences were observed between C24 and Col-0; subsequent gene ontology analysis of up-regulated genes identified SA defences and innate immune response genes, but also highlighted differential up-regulation of a number of HEAT SHOCK PROTEIN (HSP) and HEAT SHOCK TRANSCRIPTION FACTOR genes (HSF genes; HSFA2, HSFA3, and HSFB1; Bechtold et al., 2010; Fig. 2). The induction of heat stress-related genes could be directly linked to the elevated leaf temperatures observed in C24 (Bechtold et al., 2010). Furthermore, during a heat treatment (3 h at 38 °C), gene expression patterns showed high levels of accession specificity, where only three of the 35 most commonly reported heat shock-responsive transcription factors had an altered activity profile in C24 compared with seven in Col-0 (Barah et al., 2013). Unfortunately, this study does not describe the physiological consequences of the applied heat stress, and therefore it is impossible at present to conclude whether differences in gene expression led to altered phenotypic responses, namely thermotolerance at the rosette stage. Generally gene expression differences were observed between Col-0 and C24 under normal growth conditions (Bechtold et al., 2010; Xu et al., 2015), and up-regulated genes are mostly associated with defence, immune, and stress responses including PR-1, WRKY, and MYB transcription factor genes (Bechtold et al., 2010; Fig. 2). The gene expression differences observed may be explained by variations in H3K27 trimethylation between Col-0 and C24, already under non-stressed conditions. Furthermore, the majority of methylation differences occurred in genic regions which negatively correlate with gene expression between both accessions (Yang et al., 2016). Changes in H3K27 trimethylation due to a mutation in a SET domain methyltransferase gene (CLF) also resulted in differential activation and repression of stress-responsive genes in C24 (Yang et al., 2016), linking altered gene expression levels to abiotic stress responses. These differences in gene expression may to some extent explain the observed stress tolerance phenotypes. However, physiological changes such as reduced operational stomatal conductance that are balanced with high levels of photosynthetic carbon assimilation (Bechtold et al., 2010; Ferguson et al., 2018), are more difficult to explain based on gene expression data alone. The distinct physiological differences may perhaps be more closely connected to the altered plant growth and development phenotype, as discussed below. The interaction between plant growth, development, and stress responses in C24 Biomass accumulation is linked to stomatal aperture size and leaf area (Monteith and Moss, 1977; Monteith, 1994), indicating that there may be an inevitable compromise between biomass accumulation and stress tolerances associated with stomatal aperture, such as ozone, drought, heat, and pathogens (discussed above). This compromise is most notable in the reduced vegetative biomass observed in C24, and highlights a general issue for Arabidopsis research, where rosette biomass is often used as a measure of fitness and potential costs incurred due to constitutive stress tolerances (Todesco et al., 2010; Miller et al., 2015). Vegetative biomass production has been extensively studied in a Col-0×C24 RIL population (Törjék et al., 2006), and a number of metabolic and biomass QTLs have been found to overlap, where metabolic composition is related to growth/biomass accumulation (Lisec et al., 2008), and a specific metabolite combination can be used to predict vegetative biomass (Meyer et al., 2007). Hybrid growth vigour det ermined by rosette biomass in F1 hybrids derived from C24 and Col-0 was linked to the repression of diurnally regulated stress-responsive genes and the up-regulation of photosynthetic genes (Miller et al., 2015). Yet despite the different biotic and abiotic stress resistances and a reduced vegetative growth phenotype similar to cpr6-1 (Bechtold et al., 2010), seed yield is not greatly affected in C24 under water-replete and -limited conditions. Moreover partitioning of biomass into seeds is significantly increased (Bechtold et al., 2010; Ferguson et al., 2018). Particularly in the context of resource use and resource distribution, larger vegetative biomass production does not always mean better productivity (George-Jaeggli et al., 2017), which is evident in C24, where maintenance of seed weight in combination with an overall reduction in vegetative biomass and water use leads to a superior water productivity (total seed biomass per unit water) in C24 (Bechtold et al., 2010). In the case of high vegetative biomass crops, namely lignocellulose biofuel crops such as Miscanthus, switchgrass, or Sorghum, preferential resource allocation into seed at the expense of the vegetative parts is counterproductive. However, high vegetative biomass productivity also means increased water demand potentially leading to a greater reduction in soil water reserves during low rainfall, impacting hydrological cycles, thus requiring careful choice of cultivation sites (Hickman et al., 2010; Yaeger et al., 2013; McCalmont et al., 2017). We argue that mechanisms to improve water use strategies and disease resistance are also highly relevant, but may need to be coupled with vegetative biomass productivity in biofuel crops to ensure a sustainable productivity. Different life cycle strategies are rarely considered when studying adaptation and responses to abiotic stress (Caicedo et al., 2004; Dittmar et al., 2014; Bac-Molenaar et al., 2015b). For example, winter annuals mostly occur in temperate areas, whereas summer annuals occur in warmer regions (Johanson et al., 2000; Michaels et al., 2003); consequently, the different life cycle strategies are believed to be at the core of the adaptiveness of Arabidopsis (Shindo et al., 2007). Despite its presumed Portuguese origin, C24 possess a functional allele of FRIGIDA (FRI) which would normally require a period of vernalization to transition to flowering. However, the FLOWERING LOCUS C (FLC) allele of C24 is weak, therefore the vernalization requirement of C24-FRI is redundant (Michaels et al., 2003). The FRI and FLC alleles of the Col-0 accession are opposite in their functionality, that is to say that Col-0 harbours non-functional and active alleles of FRI and FLC, respectively (Johanson et al., 2000). Therefore, the active Col-FLC allele prevents noticeably early flowering, whereas the non-functional Col-FRI allele forgoes the vernalization requirement. The opposing allelic forms of FRI and FLC in Col-0 and C24 explain their similar flowering times under non-vernalizing conditions (Bechtold et al., 2010; Ferguson et al., 2018). A link between life cycle and water use strategies has been observed many times, however not always in a consistent manner. A positive genetic correlation between flowering time and water use efficiency (WUE) has often been reported (McKay et al., 2003; Easlon et al., 2014), indicating that late-flowering accessions have higher WUE compared with early-flowering accessions. While these studies concluded that late-flowering accessions have reduced water use, other studies found a negative genetic correlation between flowering time and water content (Loudet et al., 2002, 2003). It was hypothesized that FLC controls the circadian rhythm of leaf movement and therefore may also impact on the regulation of stomatal transpiration (Edwards et al., 2006). Interestingly, the accession Shahdara, which originates from a dry, high- altitude environment in Central Asia (Loudet et al., 2005), has a non-functional allele of FLC, leading to a reduced flowering time, which contributes to an increased water content (Loudet et al., 2002, 2003). Similarly, C24 possesses a non-functional allele of FLC (Michaels et al., 2003), and exhibits a high relative water content (RWC) coupled with low stomatal conductance (Bechtold et al., 2010). The notion that the non-functional FLC allele in C24 could contribute to the overall lowered stomatal conductance is intriguing. However, other development-associated genes have been identified to contribute to stomatal function, stress tolerance, and altered plant development in Arabidopsis and other plant species, such as ERECTA (Masle et al., 2005; Villagarcia et al., 2012; Shen et al., 2015), SHORT VEGETATIVE PROTEIN (SVP or AGL22; Bechtold et al., 2016), and HEAT SHOCK TRANSCRIPTION FACTOR A1b (Bechtold et al., 2013; Albihlal et al., 2018). This may therefore point to a more general association between plant development, stress tolerance, and stomatal function. A noticeable but perhaps not unsurprising finding from a recent study suggests that accessions with the least daily water use have the smallest vegetative biomass and the shortest flowering times (e.g. C24 and Ct-1) but produced the greatest amount of reproductive biomass (Ferguson et al., 2018). This points towards a trade-off between vegetative and reproductive biomass allocation in Arabidopsis, similar to that observed in its outcrossing close relative Arabidopsis lyrata (Remington et al., 2013). This trade-off and its tight association with water use indicates that it is feasible to combine reduced water use while maintaining productivity. Our recent study of 35 widely dispersed Arabidopsis accessions has demonstrated that C24 is unique in its capacity to combine low water use, high reproductive biomass, and rosette drought tolerance, with none of the other 34 accessions carrying this specific combination (Ferguson et al., 2018; Fig. 2). When this is taken into consideration with its additional broad disease resistance and tolerance to multiple abiotic stressors, C24 emerges as a highly distinctive accession (Fig. 2). Definitions of abiotic stress tolerance and how this influences strategies for engineering stress tolerance The duration and magnitude of stress determine the response and severity of associated symptoms. It is essential for plants finely to balance stress responses and growth, since diverting resources toward such responses to an extent that is beyond the duration of the experienced stress can be unfavourable in terms of growth and productivity. It is here that the defining stress tolerance becomes very important. The definition of stress tolerance is highly variable; for example, it can range from the ability of plants to survive severe stress for a few hours to the ability to maintain photosynthetic activity under stressful conditions for extended periods of the growing season. It is quite clear that if a plant cannot survive stress, it will not reproduce, and therefore survival is a form of stress tolerance. However, the ability to survive in this instance does not equate with the maintenance of productivity (Passioura, 2007). For example, protection mechanisms against water deficits are most often physiologically associated with a reduction in biomass accumulation and hence yield potential, even under water-replete conditions (Blum, 2005, 2009; Sinclair and Purcell, 2005). In addition, many studies reporting abiotic stress resistance do so based on experiments conducted under extreme artificial conditions, such as very high salinity or severe dehydration, where recovery after the stress is used as an indication of tolerance. However, under natural conditions, plants must cope with multiple environmental stresses which may vary in time, duration, and intensity. Therefore, an important aspect to consider when developing abiotic stress tolerance is how to determine the success of a transgenic plant or genotype of interest. From a physiological perspective, survival (or recovery) is the major trait representing plant stress tolerance; however, from an agronomical standpoint, yield should be the key determinant of successful stress tolerance. The challenge of scaling from model to crop Transgenic approaches manipulating single genes to engineer plants for enhanced abiotic stress tolerance have been carried out. These range from manipulating regulatory elements at the top of signalling cascades (transcription factors, kinases), to direct effectors such as antioxidant enzymes, heat shock proteins, or osmo-protectants (Zhang et al., 2011; Bechtold et al., 2013; Nakabayashi et al., 2014; Okuma et al., 2014; Stief et al., 2014; Mickelbart et al., 2015; Wu et al., 2016). However, engineering stress tolerance is often unpredictable due to existing crosstalk and the redundancy of stress tolerance pathways (Fujita et al., 2006; Friedel et al., 2012). For example, transcription factors control the expression of hundreds of downstream genes and, even though overexpression of transcription factors has led to an ever-increasing number of stress-tolerant plants, it has often come at a cost mainly through stunted growth under non-stress conditions (Kasuga et al., 1999; Tian et al., 2003; van Hulten et al., 2006; Koh et al., 2007; Todesco et al., 2010; Morran et al., 2011). Conversely overexpression of transcription factors has also led to improved stress tolerance without apparent deleterious growth effects on the plant, highlighting the unpredictable nature of this type of manipulation. For example, constitutive overexpression of AtHSFA1b in Arabidopsis improved heat and drought tolerance as well as biotrophic pathogen resistance, while at the same time improving reproductive output (Bechtold et al., 2013). This increase in reproductive output was replicated by overexpression of AtHSFA1b in Brassica napus (Bechtold et al., 2013). Similarly, transgenic rice overexpressing CBF3/DREB1A or ABF3 showed no deleterious growth effects and enhanced dehydration stress tolerance (Oh et al., 2005). Generally, negative effects on plant development can be avoided and stress tolerance greatly improved by placing transcription factor gene expression, such as that of DREB1A, under the control of a stress-inducible promoter (Kasuga et al., 1999; Pellegrineschi et al., 2004). Yet when we bear in mind an agronomic-centric stress tolerance definition (as discussed above), it has been argued that such manipulations have had limited success producing abiotic stress- tolerant cultivars, especially with regards to improving crop water productivity (Passioura, 2007). This is partially reflected by the relative lack of translation of fundamental research activities into breeding programmes designed around directly selecting for improved abiotic stress tolerance (Gilliham et al., 2017). Nevertheless, these transgenic-based studies have highlighted that tailored expression of a single gene can have profound effects on functioning of the whole plant, and any study that tests the potential phenotype of genes for alterations in stress responses provides useful information on gene function and its practicality for future applications. Conclusions One of the fundamental challenges that faces those concerned with the development of elite crop cultivars is how effectively to harness the molecular understanding of abiotic stress response pathways to engineer crops combining traits that facilitate environmental stability, resource use efficiency, and high productivity. Climate change and declining resource availabilities necessitate that the varieties of the future continue to produce maximal yields in the face of increasing occurrences of abiotic stresses and reduced resource inputs. We suggest that effective examination of natural variation of ‘undomesticated species’ can be the key to understand the molecular basis of uniting these key traits. The Arabidopsis accession C24 provides substantial evidence that productivity need not be comprised to achieve these goals, which supports the notion of a continued co-ordination between growth and defence processes to optimize productivity in complex environments (Kliebenstein, 2016). Dynamic and strong natural selection is undoubtedly central to C24’s ability to fine-tune growth and defence effectively, but it is only by developing a better understanding of how these processes are co- ordinated that we may appreciate how plant fitness is maximized in nature. This complex form of selection is not mirrored by modern day crop breeding, as it has largely developed varieties that are adapted to benign environments. So, while information obtained from understanding the responses and tolerances to environmental stresses in crop species is undoubtedly key to developing tomorrow’s elite cultivars, the natural variation present in wild species may also provide a fruitful path to deciphering the mechanisms through which such tolerances and responses are combined in a fashion that does not lead to mutual antagonism between the different traits. References Achard P . 2006 . Integration of plant responses to environmentally activated phytohormonal signals . Science 311 , 91 – 94 . Google Scholar CrossRef Search ADS Achard P , Baghour M , Chapple A , Hedden P , Van Der Straeten D , Genschik P , Moritz T , Harberd NP . 2007 . The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes . Proceedings of the National Academy of Sciences, USA 104 , 6484 – 6489 . Google Scholar CrossRef Search ADS Achard P , Gong F , Cheminant S , Alioua M , Hedden P , Genschik P . 2008 . The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism . The Plant Cell 20 , 2117 – 2129 . Google Scholar CrossRef Search ADS Albihlal WS , Chernukhin I , Blein T , Persad R , Obomighie I , Crespi M , Bechtold U , Mullineaux PM . 2018 . Arabidopsis heat shock transcription factorA1b regulates multiple developmental genes under growth and stress conditions . Journal of Experimental Botany 69 , XXX – XXX . Aliniaeifard S , van Meeteren U . 2014 . Natural variation in stomatal response to closing stimuli among Arabidopsis thaliana accessions after exposure to low VPD as a tool to recognize the mechanism of disturbed stomatal functioning . Journal of Experimental Botany 65 , 6529 – 6542 . Google Scholar CrossRef Search ADS Alonso-Blanco C , Koornneef M . 2000 . Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics . Trends in Plant Science 5 , 22 – 29 . Google Scholar CrossRef Search ADS Alvey L , Harberd NP . 2005 . DELLA proteins: integrators of multiple plant growth regulatory inputs ? Physiologia Plantarum 123 , 153 – 160 . Google Scholar CrossRef Search ADS Anderegg WR , Hicke JA , Fisher RA et al. 2015 . Tree mortality from drought, insects, and their interactions in a changing climate . New Phytologist 208 , 674 – 683 . Google Scholar CrossRef Search ADS Anderson JT . 2016 . Plant fitness in a rapidly changing world . New Phytologist 210 , 81 – 87 . Google Scholar CrossRef Search ADS Ariizumi T , Hauvermale AL , Nelson SK , Hanada A , Yamaguchi S , Steber CM . 2013 . Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling . Plant Physiology 162 , 2125 – 2139 . Google Scholar CrossRef Search ADS Bac-Molenaar JA , Fradin EF , Becker FF , Rienstra JA , van der Schoot J , Vreugdenhil D , Keurentjes JJ . 2015a . Genome-wide association mapping of fertility reduction upon heat stress reveals developmental stage-specific QTLs in Arabidopsis thaliana . The Plant Cell 27 , 1857 – 1874 . Google Scholar CrossRef Search ADS Bac-Molenaar JA , Granier C , Keurentjes JJ , Vreugdenhil D . 2015b . Genome-wide association mapping of time-dependent growth responses to moderate drought stress in Arabidopsis . Plant, Cell and Environment 39 , 88 – 102 . Google Scholar CrossRef Search ADS Barah P , Jayavelu ND , Mundy J , Bones AM . 2013 . Genome scale transcriptional response diversity among ten ecotypes of Arabidopsis thaliana during heat stress . Frontiers in Plant Science 4 , 532 . Google Scholar CrossRef Search ADS Barth S , Busimi AK , Friedrich Utz H , Melchinger AE . 2003 . Heterosis for biomass yield and related traits in five hybrids of Arabidopsis thaliana L. Heynh . Heredity 91 , 36 – 42 . Google Scholar CrossRef Search ADS Bateman RM , Crane PR , DiMichele WA , Kenrick PR , Rowe NP , Speck T , Stein WE . 1998 . Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation . Annual Review of Ecology and Systematics 29 , 263 – 292 . Google Scholar CrossRef Search ADS Baxter A , Mittler R , Suzuki N . 2014 . ROS as key players in plant stress signalling . Journal of Experimental Botany 65 , 1229 – 1240 . Google Scholar CrossRef Search ADS Bechtold U , Albihlal WS , Lawson T et al. 2013 . Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection . Journal of Experimental Botany 64 , 3467 – 3481 . Google Scholar CrossRef Search ADS Bechtold U , Lawson T , Mejia-Carranza J , Meyer RC , Brown IR , Altmann T , Ton J , Mullineaux PM . 2010 . Constitutive salicylic acid defences do not compromise seed yield, drought tolerance and water productivity in the Arabidopsis accession C24 . Plant, Cell and Environment 33 , 1959 – 1973 . Google Scholar CrossRef Search ADS Bechtold U , Penfold CA , Jenkins DJ et al. 2016 . Time-series transcriptomics reveals that AGAMOUS-LIKE22 affects primary metabolism and developmental processes in drought-stressed Arabidopsis . The Plant Cell 28 , 345 – 366 . Google Scholar CrossRef Search ADS Beerling DJ , Osborne CP , Chaloner WG . 2001 . Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era . Nature 410 , 352 – 354 . Google Scholar CrossRef Search ADS Blum A . 2005 . Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive ? Australian Journal of Agricultural Research 56 , 1159 – 1168 . Google Scholar CrossRef Search ADS Blum A . 2009 . Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress . Field Crops Research 112 , 119 – 123 . Google Scholar CrossRef Search ADS Boatwright JL , Pajerowska-Mukhtar K . 2013 . Salicylic acid: an old hormone up to new tricks . Molecular Plant Pathology 14 , 623 – 634 . Google Scholar CrossRef Search ADS Bouchabke O , Chang F , Simon M , Voisin R , Pelletier G , Durand-Tardif M . 2008 . Natural variation in Arabidopsis thaliana as a tool for highlighting differential drought responses . PLoS One 3 , e1705 . Google Scholar CrossRef Search ADS Boyer JS . 1982 . Plant productivity and environment . Science 218 , 443 – 448 . Google Scholar CrossRef Search ADS Brachi B , Faure N , Horton M , Flahauw E , Vazquez A , Nordborg M , Bergelson J , Cuguen J , Roux F . 2010 . Linkage and association mapping of Arabidopsis thaliana flowering time in nature . PLoS Genetics 6 , e1000940 . Google Scholar CrossRef Search ADS Brosché M , Merilo E , Mayer F , Pechter P , Puzõrjova I , Brader G , Kangasjärvi J , Kollist H . 2010 . Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance . Plant, Cell and Environment 33 , 914 – 925 . Google Scholar CrossRef Search ADS Brossa R , López-Carbonell M , Jubany-Marí T , Alegre L . 2011 . Interplay between abscisic acid and jasmonic acid and its role in water-oxidative stress in wild-type, ABA-deficient, JA-deficient, and ascorbate-deficient Arabidopsis plants . Journal of Plant Growth Regulation 30 , 322 – 333 . Google Scholar CrossRef Search ADS Caicedo AL , Stinchcombe JR , Olsen KM , Schmitt J , Purugganan MD . 2004 . Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait . Proceedings of the National Academy of Sciences, USA 101 , 15670 – 15675 . Google Scholar CrossRef Search ADS Campos ML , Yoshida Y , Major IT et al. 2016 . Rewiring of jasmonate and phytochrome B signalling uncouples plant growth–defense tradeoffs . Nature Communications 7 , 12570 . Google Scholar CrossRef Search ADS Cerrudo I , Caliri-Ortiz ME , Keller MM , Degano ME , Demkura PV , Ballaré CL . 2017 . Exploring growth–defence trade-offs in Arabidopsis: phytochrome B inactivation requires JAZ10 to suppress plant immunity but not to trigger shade-avoidance responses . Plant, Cell and Environment 40 , 635 – 644 . Google Scholar CrossRef Search ADS Chaves MM , Flexas J , Pinheiro C . 2009 . Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell . Annals of Botany 103 , 551 – 560 . Google Scholar CrossRef Search ADS Chumakov MI , Kurbanova IV , Solovova GK . 2002 . Agrobacterial transformation of uninjured plants . Russian Journal of Plant Physiology 49 , 799 – 803 . Google Scholar CrossRef Search ADS Clarke SM , Cristescu SM , Miersch O , Harren FJ , Wasternack C , Mur LA . 2009 . Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana . New Phytologist 182 , 175 – 187 . Google Scholar CrossRef Search ADS Clarke SM , Mur LA , Wood JE , Scott IM . 2004 . Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana . The Plant Journal 38 , 432 – 447 . Google Scholar CrossRef Search ADS Colebrook EH , Thomas SG , Phillips AL , Hedden P . 2014 . The role of gibberellin signalling in plant responses to abiotic stress . Journal of Experimental Biology 217 , 67 – 75 . Google Scholar CrossRef Search ADS Compant S , van der Heijden MG , Sessitsch A . 2010 . Climate change effects on beneficial plant–microorganism interactions . FEMS Microbiology Ecology 73 , 197 – 214 . Cramer GR , Urano K , Delrot S , Pezzotti M , Shinozaki K . 2011 . Effects of abiotic stress on plants: a systems biology perspective . BMC Plant Biology 11 , 163 . Google Scholar CrossRef Search ADS Crawford AJ , McLachlan DH , Hetherington AM , Franklin KA . 2012 . High temperature exposure increases plant cooling capacity . Current Biology 22 , R396 – R397 . Google Scholar CrossRef Search ADS Cutler SR , Rodriguez PL , Finkelstein RR , Abrams SR . 2010 . Abscisic acid: emergence of a core signaling network . Annual Review of Plant Biology 61 , 651 – 679 . Google Scholar CrossRef Search ADS de Ollas C , Arbona V , Gómez-Cadenas A . 2015 . Jasmonoyl isoleucine accumulation is needed for abscisic acid build-up in roots of Arabidopsis under water stress conditions . Plant, Cell and Environment 38 , 2157 – 2170 . Google Scholar CrossRef Search ADS Dittmar EL , Oakley CG , Ågren J , Schemske DW . 2014 . Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value . Molecular Ecology 23 , 4291 – 4303 . Google Scholar CrossRef Search ADS Easlon HM , Nemali KS , Richards JH , Hanson DT , Juenger TE , McKay JK . 2014 . The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana . Photosynthesis Research 119 , 119 – 129 . Google Scholar CrossRef Search ADS Edwards KD , Anderson PE , Hall A , Salathia NS , Locke JC , Lynn JR , Straume M , Smith JQ , Millar AJ . 2006 . FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock . The Plant Cell 18 , 639 – 650 . Google Scholar CrossRef Search ADS Eichmann R , Schäfer P . 2015 . Growth versus immunity—a redirection of the cell cycle ? Current Opinion in Plant Biology 26 , 106 – 112 . Google Scholar CrossRef Search ADS Feng S , Martinez C , Gusmaroli G et al. 2008 . Coordinated regulation of Arabidopsis thaliana development by light and gibberellins . Nature 451 , 475 – 479 . Google Scholar CrossRef Search ADS Ferguson JN , Humphry M , Lawson T , Oliver B , Bechtold U . 2018 . Natural variation of life-history traits, water use, and drought responses in Arabidopsis . Plant Direct 2 , e00035 . Google Scholar CrossRef Search ADS Friedel S , Usadel B , von Wirén N , Sreenivasulu N . 2012 . Reverse engineering: a key component of systems biology to unravel global abiotic stress cross-talk . Frontiers in Plant Science 3 , 294 . Google Scholar CrossRef Search ADS Fujimoto R , Taylor JM , Shirasawa S , Peacock WJ , Dennis ES . 2012 . Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity . Proceedings of the National Academy of Sciences, USA 109 , 7109 – 14 . Google Scholar CrossRef Search ADS Fujita M , Fujita Y , Noutoshi Y , Takahashi F , Narusaka Y , Yamaguchi-Shinozaki K , Shinozaki K . 2006 . Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks . Current Opinion in Plant Biology 9 , 436 – 442 . Google Scholar CrossRef Search ADS Fujita Y , Fujita M , Shinozaki K , Yamaguchi-Shinozaki K . 2011 . ABA-mediated transcriptional regulation in response to osmotic stress in plants . Journal of Plant Research 124 , 509 – 525 . Google Scholar CrossRef Search ADS Fujita Y , Yoshida T , Yamaguchi-Shinozaki K . 2013 . Pivotal role of the AREB/ABF–SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants . Physiologia Plantarum 147 , 15 – 27 . Google Scholar CrossRef Search ADS Gallego-Bartolome J , Minguet EG , Grau-Enguix F , Abbas M , Locascio A , Thomas SG , Alabadi D , Blazquez MA . 2012 . Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis . Proceedings of the National Academy of Sciences, USA 109 , 13446 – 13451 . Google Scholar CrossRef Search ADS Galvez-Valdivieso G , Mullineaux PM . 2010 . The role of reactive oxygen species in signalling from chloroplasts to the nucleus . Physiologia Plantarum 138 , 430 – 439 . Google Scholar CrossRef Search ADS Gao D , Appiano M , Huibers RP , Loonen AE , Visser RG , Wolters AM , Bai Y . 2015 . Natural loss-of-function mutation of EDR1 conferring resistance to tomato powdery mildew in Arabidopsis thaliana accession C24 . Molecular Plant Pathology 16 , 71 – 82 . Google Scholar CrossRef Search ADS George-Jaeggli B , Mortlock MY , Borrell AK . 2017 . Bigger is not always better: reducing leaf area helps stay-green sorghum use soil water more slowly . Environmental and Experimental Botany 138 , 119 – 129 . Google Scholar CrossRef Search ADS Gepts P . 2010 . Crop domestication as a long-term selection experiment . Plant Breeding Reviews 1 – 44 . Ghedira R , De Buck S , Nolf J , Depicker A . 2013 . The efficiency of Arabidopsis thaliana floral dip transformation is determined not only by the Agrobacterium strain used but also by the physiology and the ecotype of the dipped plant . Molecular Plant-Microbe Interactions 26 , 823 – 832 . Google Scholar CrossRef Search ADS Gilley A , Fletcher RA . 1998 . Gibberellin antagonizes paclobutrazol-induced stress protection in wheat seedlings . Journal of Plant Physiology 153 , 200 – 207 . Google Scholar CrossRef Search ADS Gilliham M , Able JA , Roy SJ . 2017 . Translating knowledge about abiotic stress tolerance to breeding programmes . The Plant Journal 90 , 898 – 917 . Google Scholar CrossRef Search ADS Golldack D , Li C , Mohan H , Probst N . 2013 . Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions . Plant Cell Reports 32 , 1007 – 1016 . Google Scholar CrossRef Search ADS Gray WM . 2004 . Hormonal regulation of plant growth and development . PLoS Biology 2 , e311 . Google Scholar CrossRef Search ADS Guisan A , Thuiller W . 2005 . Predicting species distribution: offering more than simple habitat models . Ecology Letters 8 , 993 – 1009 . Google Scholar CrossRef Search ADS Hancock JF . 2005 . Contributions of domesticated plant studies to our understanding of plant evolution . Annals of Botany 96 , 953 – 963 . Google Scholar CrossRef Search ADS Hannah MA , Wiese D , Freund S , Fiehn O , Heyer AG , Hincha DK . 2006 . Natural genetic variation of freezing tolerance in Arabidopsis . Plant Physiology 142 , 98 – 112 . Google Scholar CrossRef Search ADS Hartmann L , Pedrotti L , Weiste C et al. 2015 . Crosstalk between two bZIP signaling pathways orchestrates salt-induced metabolic reprogramming in Arabidopsis roots . The Plant Cell 27 , 2244 – 2260 . Google Scholar CrossRef Search ADS Heil M . 2014 . Trade-offs associated with induced resistance . In: Walters D , Newton A , Lyon G , eds. Induced resistance for plant defense: a sustainable approach to crop protection . Oxford : Blackwell Publishing , 171 – 192 . Heil M , Baldwin IT . 2002 . Fitness costs of induced resistance: emerging experimental support for a slippery concept . Trends in Plant Science 7 , 61 – 67 . Google Scholar CrossRef Search ADS Herms DA , Mattson WJ . 1992 . The dilemma of plants: to grow or defend . Quarterly Review of Biology 67 , 283 – 335 . Google Scholar CrossRef Search ADS Hey SJ , Byrne E , Halford NG . 2010 . The interface between metabolic and stress signalling . Annals of Botany 105 , 197 – 203 . Google Scholar CrossRef Search ADS Hickman GC , VanLoocke A , Dohleman FG , Bernacchi CJ . 2010 . A comparison of canopy evapotranspiration for maize and two perennial grasses identified as potential bioenergy crops . GCB Bioenergy 2 , 157 – 168 . Holman IP , Brown C , Janes V , Sandars D . 2017 . Can we be certain about future land use change in Europe? A multi-scenario, integrated-assessment analysis . Agricultural Systems 151 , 126 – 135 . Google Scholar CrossRef Search ADS Horváth E , Csiszár J , Gallé Á , Poór P , Szepesi Á , Tari I . 2015 . Hardening with salicylic acid induces concentration-dependent changes in abscisic acid biosynthesis of tomato under salt stress . Journal of Plant Physiology 183 , 54 – 63 . Google Scholar CrossRef Search ADS Horváth E , Szalai G , Janda T . 2007 . Induction of abiotic stress tolerance by salicylic acid signaling . Journal of Plant Growth Regulation 26 , 290 – 300 . Google Scholar CrossRef Search ADS Hoshika Y , Katata G , Deushi M , Watanabe M , Koike T , Paoletti E . 2015 . Ozone-induced stomatal sluggishness changes carbon and water balance of temperate deciduous forests . Scientific Reports 5 , 9871 . Google Scholar CrossRef Search ADS Hou X , Ding L , Yu H . 2013 . Crosstalk between GA and JA signaling mediates plant growth and defense . Plant Cell Reports 32 , 1067 – 1074 . Google Scholar CrossRef Search ADS Hou X , Lee LY , Xia K , Yan Y , Yu H . 2010 . DELLAs modulate jasmonate signaling via competitive binding to JAZs . Developmental Cell 19 , 884 – 894 . Google Scholar CrossRef Search ADS Jha D , Shirley N , Tester M , Roy SJ . 2010 . Variation in salinity tolerance and shoot sodium accumulation in Arabidopsis ecotypes linked to differences in the natural expression levels of transporters involved in sodium transport . Plant, Cell and Environment 33 , 793 – 804 . Johanson U , West J , Lister C , Michaels S , Amasino R , Dean C . 2000 . Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time . Science 290 , 344 – 347 . Google Scholar CrossRef Search ADS Juenger TE , Mckay JK , Hausmann N , Stowe KA , Dawson TE , Simms EL , Keurentjes JJB , Sen S , Richards JH . 2005 . Identification and characterization of QTL underlying whole plant physiology in Arabidopsis thaliana: d13C, stomatal conductance and transpiration efficiency . Plant, Cell and Environment 28 , 697 – 708 . Google Scholar CrossRef Search ADS Kangasärvi J , Talvinen J , Utriainen M , Karjalainen R . 1994 . Plant defence systems induced by ozone . Plant, Cell and Environment 17 , 783 – 794 . Google Scholar CrossRef Search ADS Kant MR , Baldwin IT . 2007 . The ecogenetics and ecogenomics of plant–herbivore interactions: rapid progress on a slippery road . Current Opinion in Genetics and Development 17 , 519 – 524 . Google Scholar CrossRef Search ADS Karssen CM , Brinkhorst-van der Swan DL , Breekland AE , Koornneef M . 1983 . Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh . Planta 157 , 158 – 165 . Google Scholar CrossRef Search ADS Kasuga M , Liu Q , Miura S , Yamaguchi-Shinozaki K , Shinozaki K . 1999 . Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor . Nature Biotechnology 17 , 287 – 291 . Google Scholar CrossRef Search ADS Kazan K . 2015 . Diverse roles of jasmonates and ethylene in abiotic stress tolerance . Trends in Plant Science 20 , 219 – 229 . Google Scholar CrossRef Search ADS Kazan K , Manners JM . 2011 . The interplay between light and jasmonate signalling during defence and development . Journal of Experimental Botany 62 , 4087 – 4100 . Google Scholar CrossRef Search ADS Khan MI , Fatma M , Per TS , Anjum NA , Khan NA . 2015 . Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants . Frontiers in Plant Science 6 , 462 . Khan MI , Iqbal N , Masood A , Per TS , Khan NA . 2013 . Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation . Plant Signaling and Behavior 8 , e26374 . Google Scholar CrossRef Search ADS Kim JS , Mizoi J , Kidokoro S et al. 2012 . Arabidopsis growth-regulating factor7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A . The Plant Cell 24 , 3393 – 3405 . Google Scholar CrossRef Search ADS Kliebenstein DJ . 2016 . False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology . Physiological and Molecular Plant Pathology 95 , 55 – 59 . Google Scholar CrossRef Search ADS Koh S , Lee SC , Kim MK , Koh JH , Lee S , An G , Choe S , Kim SR . 2007 . T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses . Plant Molecular Biology 65 , 453 – 466 . Google Scholar CrossRef Search ADS Koornneef M , Meinke D . 2010 . The development of Arabidopsis as a model plant . The Plant Journal 61 , 909 – 921 . Google Scholar CrossRef Search ADS Koricheva J , Nykänen H , Gianoli E . 2004 . Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all ? American Naturalist 163 , E64 – E75 . Google Scholar CrossRef Search ADS La Camera S , Geoffroy P , Samaha H , Ndiaye A , Rahim G , Legrand M , Heitz T . 2005 . A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis . The Plant Journal 44 , 810 – 825 . Google Scholar CrossRef Search ADS Lapin D , Meyer RC , Takahashi H , Bechtold U , Van den Ackerveken G . 2012 . Broad-spectrum resistance of Arabidopsis C24 to downy mildew is mediated by different combinations of isolate-specific loci . New Phytologist 196 , 1171 – 1181 . Google Scholar CrossRef Search ADS Lasky JR , Des Marais DL , Lowry DB , Povolotskaya I , McKay JK , Richards JH , Keitt TH , Juenger TE . 2014 . Natural variation in abiotic stress responsive gene expression and local adaptation to climate in Arabidopsis thaliana . Molecular Biology and Evolution 31 , 2283 – 2296 . Google Scholar CrossRef Search ADS Leng P , Yuan B , Guo Y . 2014 . The role of abscisic acid in fruit ripening and responses to abiotic stress . Journal of Experimental Botany 65 , 4577 – 4588 . Google Scholar CrossRef Search ADS Leone M , Keller MM , Cerrudo I , Ballaré CL . 2014 . To grow or defend? Low red:far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability . New Phytologist 204 , 355 – 367 . Google Scholar CrossRef Search ADS Lisec J , Meyer RC , Steinfath M et al. 2008 . Identification of metabolic and biomass QTL in Arabidopsis thaliana in a parallel analysis of RIL and IL populations . The Plant Journal 53 , 960 – 972 . Google Scholar CrossRef Search ADS Liu C , Ruan Y , Lin Z , Wei R , Peng Q , Guan C , Ishii H . 2008 . Antagonism between acibenzolar-S-methyl-induced systemic acquired resistance and jasmonic acid-induced systemic acquired susceptibility to Colletotrichum orbiculare infection in cucumber . Physiological and Molecular Plant Pathology 72 , 141 – 145 . Google Scholar CrossRef Search ADS Liu X , Hu P , Huang M , Tang Y , Li Y , Li L , Hou X . 2016 . The NF–YC–RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis . Nature Communications 7 , 12768 . Google Scholar CrossRef Search ADS Liu X , Rockett KS , Kørner CJ , Pajerowska-Mukhtar KM . 2015 . Salicylic acid signalling: new insights and prospects at a quarter-century milestone . Essays In Biochemistry 58 , 101 – 113 . Google Scholar CrossRef Search ADS López-Arredondo D , González-Morales SI , Bello-Bello E , Alejo-Jacuinde G , Herrera L . 2015 . Engineering food crops to grow in harsh environments . F1000 Research 4 , 651 . Loudet O , Chaillou S , Camilleri C , Bouchez D , Daniel-Vedele F . 2002 . Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis . Theoretical and Applied Genetics 104 , 1173 – 1184 . Google Scholar CrossRef Search ADS Loudet O , Chaillou S , Krapp A , Daniel-Vedele F . 2003 . Quantitative trait loci analysis of water and anion contents in interaction with nitrogen availability in Arabidopsis thaliana . Genetics 163 , 711 – 722 . Loudet O , Gaudon V , Trubuil A , Daniel-Vedele F . 2005 . Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family . Theoretical and Applied Genetics 110 , 742 – 753 . Google Scholar CrossRef Search ADS Masle J , Gilmore SR , Farquhar GD . 2005 . The ERECTA gene regulates plant transpiration efficiency in Arabidopsis . Nature 436 , 866 – 870 . Google Scholar CrossRef Search ADS McCalmont JP , Hastings A , McNamara NP , Richter GM , Robson P , Donnison IS , Clifton-Brown J . 2017 . Environmental costs and benefits of growing Miscanthus for bioenergy in the UK . Global Change Biology. Bioenergy 9 , 489 – 507 . Google Scholar CrossRef Search ADS McKay JK , Richards JH , Mitchell-Olds T . 2003 . Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits . Molecular Ecology 12 , 1137 – 1151 . Google Scholar CrossRef Search ADS McKay JK , Richards JH , Nemali KS , Sen S , Mitchell-Olds T , Boles S , Stahl EA , Wayne T , Juenger TE . 2008 . Genetics of drought adaptation in Arabidopsis thaliana II. QTL analysis of a new mapping population, KAS-1 × TSU-1 . Evolution 62 , 3014 – 3026 . Google Scholar CrossRef Search ADS Melotto M , Underwood W , Koczan J , Nomura K , He SY . 2006 . Plant stomata function in innate immunity against bacterial invasion . Cell 126 , 969 – 980 . Google Scholar CrossRef Search ADS Meyer RS , DuVal AE , Jensen HR . 2012 . Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops . New Phytologist 196 , 29 – 48 . Google Scholar CrossRef Search ADS Meyer RC , Kusterer B , Lisec J et al. 2010 . QTL analysis of early stage heterosis for biomass in Arabidopsis . Theoretical and Applied Genetics 120 , 227 – 237 . Google Scholar CrossRef Search ADS Meyer RC , Steinfath M , Lisec J et al. 2007 . The metabolic signature related to high plant growth rate in Arabidopsis thaliana . Proceedings of the National Academy of Sciences, USA 104 , 4759 – 64 . Google Scholar CrossRef Search ADS Michaels SD , He Y , Scortecci KC , Amasino RM . 2003 . Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis . Proceedings of the National Academy of Sciences, USA 100 , 10102 – 7 . Google Scholar CrossRef Search ADS Mickelbart MV , Hasegawa PM , Bailey-Serres J . 2015 . Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability . Nature Reviews. Genetics 16 , 237 – 251 . Google Scholar CrossRef Search ADS Miller M , Song Q , Shi X , Juenger TE , Chen ZJ . 2015 . Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis . Nature Communications 6 , 7453 . Google Scholar CrossRef Search ADS Mills G , Hayes F , Wilkinson S , Davies WJ . 2009 . Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species . Global Change Biology 15 , 1522 – 1533 . Google Scholar CrossRef Search ADS Mittler R . 2006 . Abiotic stress, the field environment and stress combination . Trends in Plant Science 11 , 15 – 19 . Google Scholar CrossRef Search ADS Miura K , Okamoto H , Okuma E , Shiba H , Kamada H , Hasegawa PM , Murata Y . 2013 . SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis . The Plant Journal 73 , 91 – 104 . Google Scholar CrossRef Search ADS Miura K , Tada Y . 2014 . Regulation of water, salinity, and cold stress responses by salicylic acid . Frontiers in Plant Science 5 , 4 . Google Scholar CrossRef Search ADS Mommer L , Wolters-Arts M , Andersen C , Visser EJ , Pedersen O . 2007 . Submergence-induced leaf acclimation in terrestrial species varying in flooding tolerance . New Phytologist 176 , 337 – 345 . Google Scholar CrossRef Search ADS Monteith JL . 1994 . Validity of the correlation between intercepted radiation and biomass . Agricultural and Forest Meteorology 68 , 213 – 220 . Google Scholar CrossRef Search ADS Monteith JL , Moss CJ . 1977 . Climate and the efficiency of crop production in Britain [and discussion] . Philosophical Transactions of the Royal Society B: Biological Sciences 281 , 277 – 294 . Google Scholar CrossRef Search ADS Morran S , Eini O , Pyvovarenko T , Parent B , Singh R , Ismagul A , Eliby S , Shirley N , Langridge P , Lopato S . 2011 . Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors . Plant Biotechnology Journal 9 , 230 – 249 . Google Scholar CrossRef Search ADS Muñoz-Bertomeu J , Bermúdez MA , Segura J , Ros R . 2011 . Arabidopsis plants deficient in plastidial glyceraldehyde-3-phosphate dehydrogenase show alterations in abscisic acid (ABA) signal transduction: interaction between ABA and primary metabolism . Journal of Experimental Botany 62 , 1229 – 1239 . Google Scholar CrossRef Search ADS Muñoz-Espinoza VA , López-Climent MF , Casaretto JA , Gómez-Cadenas A . 2015 . Water stress responses of tomato mutants impaired in hormone biosynthesis reveal abscisic acid, jasmonic acid and salicylic acid interactions . Frontiers in Plant Science 6 , 997 . Google Scholar CrossRef Search ADS Nakabayashi R , Yonekura-Sakakibara K , Urano K et al. 2014 . Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids . The Plant Journal 77 , 367 – 379 . Google Scholar CrossRef Search ADS Normand S , Treier UA , Randin C , Vittoz P , Guisan A , Svenning J-C . 2009 . Importance of abiotic stress as a range-limit determinant for European plants: insights from species responses to climatic gradients . Global Ecology and Biogeography 18 , 437 – 449 . Google Scholar CrossRef Search ADS Oh SJ , Song SI , Kim YS , Jang HJ , Kim SY , Kim M , Kim YK , Nahm BH , Kim JK . 2005 . Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth . Plant Physiology 138 , 341 – 351 . Google Scholar CrossRef Search ADS Okuma E , Nozawa R , Murata Y , Miura K . 2014 . Accumulation of endogenous salicylic acid confers drought tolerance to Arabidopsis . Plant Signaling and Behavior 9 , e28085 . Google Scholar CrossRef Search ADS Osborne SA , Mills G , Hayes F ,et al. . 2016 . Has the sensitivity of soybean cultivars to ozone pollution increased with time? An analysis of published dose–response data . Global Change Biology 22 , 3097 – 3111 . Google Scholar CrossRef Search ADS Overmyer K , Brosché M , Pellinen R et al. 2005 . Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant . Plant Physiology 137 , 1092 – 1104 . Google Scholar CrossRef Search ADS Pantin F , Monnet F , Jannaud D , Costa JM , Renaud J , Muller B , Simonneau T , Genty B . 2013 . The dual effect of abscisic acid on stomata . New Phytologist 197 , 65 – 72 . Google Scholar CrossRef Search ADS Paoletti E , Grulke NE . 2010 . Ozone exposure and stomatal sluggishness in different plant physiognomic classes . Environmental Pollution 158 , 2664 – 2671 . Google Scholar CrossRef Search ADS Passioura J . 2007 . The drought environment: physical, biological and agricultural perspectives . Journal of Experimental Botany 58 , 113 – 117 . Google Scholar CrossRef Search ADS Pautasso M , Doring TF , Garbelotto M , Pellis L , Jeger MJ . 2012 . Impacts of climate change on plant diseases—opinions and trends . European Journal of Plant Pathology 133 , 295 – 313 . Google Scholar CrossRef Search ADS Pauwels L , Morreel K , De Witte E , Lammertyn F , Van Montagu M , Boerjan W , Inze D , Goossens A . 2008 . Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells . Proceedings of the National Academy of Sciences, USA 105 , 1380 – 1385 . Google Scholar CrossRef Search ADS Pellegrineschi A , Reynolds M , Pacheco M , Brito RM , Almeraya R , Yamaguchi-Shinozaki K , Hoisington D . 2004 . Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions . Genome 47 , 493 – 500 . Google Scholar CrossRef Search ADS Peng J , Carol P , Richards DE , King KE , Cowling RJ , Murphy GP , Harberd NP . 1997 . The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses . Genes and Development 11 , 3194 – 3205 . Google Scholar CrossRef Search ADS Peters K , Breitsameter L , Gerowitt B . 2014 . Impact of climate change on weeds in agriculture: a review . Agronomy for Sustainable Development 34 , 707 – 721 . Google Scholar CrossRef Search ADS Petrov V , Hille J , Mueller-Roeber B , Gechev TS . 2015 . ROS-mediated abiotic stress-induced programmed cell death in plants . Frontiers in Plant Science 6 , 69 . Google Scholar CrossRef Search ADS Prinzenberg AE , Barbier H , Salt DE , Stich B , Reymond M . 2010 . Relationships between growth, growth response to nutrient supply, and ion content using a recombinant inbred line population in Arabidopsis . Plant Physiology 154 , 1361 – 1371 . Google Scholar CrossRef Search ADS Rademacher W . 2000 . Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways . Annual Review of Plant Physiology and Plant Molecular Biology 51 , 501 – 531 . Google Scholar CrossRef Search ADS Raghavendra AS , Gonugunta VK , Christmann A , Grill E . 2010 . ABA perception and signalling . Trends in Plant Science 15 , 395 – 401 . Google Scholar CrossRef Search ADS Rejeb IB , Pastor V , Mauch-Mani B . 2014 . Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms . Plants 3 , 458 – 475 . Google Scholar CrossRef Search ADS Remington DL , Leinonen PH , Leppälä J , Savolainen O . 2013 . Complex genetic effects on early vegetative development shape resource allocation differences between Arabidopsis lyrata populations . Genetics 195 , 1087 – 1102 . Google Scholar CrossRef Search ADS Richards DE , King KE , Ait-Ali T , Harberd NP . 2001 . How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling . Annual Review of Plant Physiology and Plant Molecular Biology 52 , 67 – 88 . Google Scholar CrossRef Search ADS Riemann M , Dhakarey R , Hazman M , Miro B , Kohli A , Nick P . 2015 . Exploring jasmonates in the hormonal network of drought and salinity responses . Frontiers in Plant Science 6 , 1077 . Google Scholar CrossRef Search ADS Rivas-San Vicente M , Plasencia J . 2011 . Salicylic acid beyond defence: its role in plant growth and development . Journal of Experimental Botany 62 , 3321 – 3338 . Google Scholar CrossRef Search ADS Rohde P , Hincha DK , Heyer AG . 2004 . Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance . The Plant Journal 38 , 790 – 799 . Google Scholar CrossRef Search ADS Sah SK , Reddy KR , Li J . 2016 . Abscisic acid and abiotic stress tolerance in crop plants . Frontiers in Plant Science 7 , 571 . Google Scholar CrossRef Search ADS Sanchez-Bermejo E , Zhu W , Tasset C , Eimer H , Sureshkumar S , Singh R , Sundaramoorthi V , Colling L , Balasubramanian S . 2015 . Genetic architecture of natural variation in thermal responses of Arabidopsis . Plant Physiology 169 , 647 – 659 . Google Scholar CrossRef Search ADS Sandermann H , Ernst D , Heller W , Langebartels C . 1998 . Ozone: an abiotic elicitor of plant defence reactions . Trends in Plant Science 3 , 47 – 50 . Google Scholar CrossRef Search ADS Santiago J , Dupeux F , Betz K , Antoni R , Gonzalez-Guzman M , Rodriguez L , Márquez JA , Rodriguez PL . 2012 . Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs . Plant Science 182 , 3 – 11 . Google Scholar CrossRef Search ADS Schmöckel SM , Garcia AF , Berger B , Tester M , Webb AA , Roy SJ . 2015 . Different NaCl-induced calcium signatures in the Arabidopsis thaliana ecotypes Col-0 and C24 . PLoS One 10 , e0117564 . Google Scholar CrossRef Search ADS Sekine KT , Kawakami S , Hase S , Kubota M , Ichinose Y , Shah J , Kang HG , Klessig DF , Takahashi H . 2008 . High level expression of a virus resistance gene, RCY1, confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana . Molecular Plant-Microbe Interactions 21 , 1398 – 1407 . Google Scholar CrossRef Search ADS Shen H , Zhong X , Zhao F et al. 2015 . Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato . Nature Biotechnology 33 , 996 – 1003 . Google Scholar CrossRef Search ADS Shindo C , Bernasconi G , Hardtke CS . 2007 . Natural genetic variation in Arabidopsis: tools, traits and prospects for evolutionary ecology . Annals of Botany 99 , 1043 – 1054 . Google Scholar CrossRef Search ADS Silva-Correia J , Freitas S , Tavares RM , Lino-Neto T , Azevedo H . 2014 . Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development . Plant Methods 10 , 7 . Google Scholar CrossRef Search ADS Sinclair TR , Purcell LC . 2005 . Is a physiological perspective relevant in a ‘genocentric’ age ? Journal of Experimental Botany 56 , 2777 – 2782 . Google Scholar CrossRef Search ADS Souza LA , Monteiro CC , Carvalho RF , Gratão PL , Azevedo RA . 2017 . Dealing with abiotic stresses: an integrative view of how phytohormones control abiotic stress-induced oxidative stress . Theoretical and Experimental Plant Physiology 29 , 109 – 127 . Google Scholar CrossRef Search ADS Stief A , Altmann S , Hoffmann K , Pant BD , Scheible WR , Bäurle I . 2014 . Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors . The Plant Cell 26 , 1792 – 1807 . Google Scholar CrossRef Search ADS Sun TP . 2010 . Gibberellin–GID1–DELLA: a pivotal regulatory module for plant growth and development . Plant Physiology 154 , 567 – 570 . Google Scholar CrossRef Search ADS Szepesi A , Csiszár J , Gémes K , Horváth E , Horváth F , Simon ML , Tari I . 2009 . Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L . Journal of Plant Physiology 166 , 914 – 925 . Google Scholar CrossRef Search ADS Takahashi H , Miller J , Nozaki Y , Sukamto , Takeda M , Shah J , Hase S , Ikegami M , Ehara Y , Dinesh-Kumar SP . 2002 . RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism . The Plant Journal 32 , 655 – 667 . Google Scholar CrossRef Search ADS Tian D , Traw MB , Chen JQ , Kreitman M , Bergelson J . 2003 . Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana . Nature 423 , 74 – 77 . Google Scholar CrossRef Search ADS Todesco M , Balasubramanian S , Hu TT et al. 2010 . Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana . Nature 465 , 632 – 636 . Google Scholar CrossRef Search ADS Ton J , Pieterse CM , Van Loon LC . 1999 . Identification of a locus in arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato . Molecular Plant-Microbe Interactions 12 , 911 – 918 . Google Scholar CrossRef Search ADS Törjék O , Witucka-Wall H , Meyer RC et al. 2006 . Segregation distortion in Arabidopsis C24/Col-0 and Col-0/C24 recombinant inbred line populations is due to reduced fertility caused by epistatic interaction of two loci . Theoretical and Applied Genetics 113 , 1551 – 1561 . Google Scholar CrossRef Search ADS Trontin C , Kiani S , Corwin JA , Hématy K , Yansouni J , Kliebenstein DJ , Loudet O . 2014 . A pair of receptor-like kinases is responsible for natural variation in shoot growth response to mannitol treatment in Arabidopsis thaliana . The Plant Journal 78 , 121 – 133 . Google Scholar CrossRef Search ADS Umezawa T , Nakashima K , Miyakawa T , Kuromori T , Tanokura M , Shinozaki K , Yamaguchi-Shinozaki K . 2010 . Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport . Plant and Cell Physiology 51 , 1821 – 1839 . Google Scholar CrossRef Search ADS van Hulten M , Pelser M , van Loon LC , Pieterse CMJ , Ton J . 2006 . Costs and benefits of priming for defense in Arabidopsis . Proceedings of the National Academy of Sciences, USA 103 , 5602 – 5607 . Google Scholar CrossRef Search ADS Vashisht D , Hesselink A , Pierik R et al. 2011 . Natural variation of submergence tolerance among Arabidopsis thaliana accessions . New Phytologist 190 , 299 – 310 . Google Scholar CrossRef Search ADS Verma V , Ravindran P , Kumar PP . 2016 . Plant hormone-mediated regulation of stress responses . BMC Plant Biology 16 , 86 . Google Scholar CrossRef Search ADS Verslues PE . 2017 . Time to grow: factors that control plant growth during mild to moderate drought stress . Plant, Cell and Environment 40 , 177 – 179 . Google Scholar CrossRef Search ADS Villagarcia H , Morin AC , Shpak ED , Khodakovskaya MV . 2012 . Modification of tomato growth by expression of truncated ERECTA protein from Arabidopsis thaliana . Journal of Experimental Botany 63 , 6493 – 6504 . Google Scholar CrossRef Search ADS Vlot AC , Dempsey DA , Klessig DF . 2009 . Salicylic acid, a multifaceted hormone to combat disease . Annual Review of Phytopathology 47 , 177 – 206 . Google Scholar CrossRef Search ADS Wang LJ , Fan L , Loescher W , Duan W , Liu GJ , Cheng JS , Luo HB , Li SH . 2010 . Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves . BMC Plant Biology 10 , 34 . Google Scholar CrossRef Search ADS Wasternack C , Hause B . 2013 . Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany . Annals of Botany 111 , 1021 – 1058 . Google Scholar CrossRef Search ADS Wu H , Fu B , Sun P , Xiao C , Liu JH . 2016 . A NAC transcription factor represses putrescine biosynthesis and affects drought tolerance . Plant Physiology 172 , 1532 – 1547 . Google Scholar CrossRef Search ADS Xu E , Vaahtera L , Hõrak H , Hincha DK , Heyer AG , Brosché M . 2015 . Quantitative trait loci mapping and transcriptome analysis reveal candidate genes regulating the response to ozone in Arabidopsis thaliana . Plant, Cell and Environment 38 , 1418 – 1433 . Google Scholar CrossRef Search ADS Yaeger MA , Sivapalan M , McIsaac GF , Cai X . 2013 . Comparative analysis of hydrologic signatures in two agricultural watersheds in east-central Illinois: legacies of the past to inform the future . Hydrology and Earth System Sciences 17 , 4607 – 4623 . Google Scholar CrossRef Search ADS Yamamoto Y . 2016 . Quality control of photosystem II: the mechanisms for avoidance and tolerance of light and heat stresses are closely linked to membrane fluidity of the thylakoids . Frontiers in Plant Science 7 , 1136 . Google Scholar CrossRef Search ADS Yang M , Wang X , Huang H et al. 2016 . Natural variation of H3K27me3 modification in two Arabidopsis accessions and their hybrid . Journal of Integrative Plant Biology 58 , 466 – 474 . Google Scholar CrossRef Search ADS Yang D-L , Yao J , Mei C-S et al. 2012 . Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade . Proceedings of the National Academy of Sciences, USA 109 , E1192 – E1200 . Google Scholar CrossRef Search ADS Ye N , Jia L , Zhang J . 2012 . ABA signal in rice under stress conditions . Rice 5 , 1 . Google Scholar CrossRef Search ADS Yoshida T , Fujita Y , Maruyama K , Mogami J , Todaka D , Shinozaki K , Yamaguchi-Shinozaki K . 2015 . Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress . Plant, Cell and Environment 38 , 35 – 49 . Google Scholar CrossRef Search ADS Zeng D-E , Hou P , Xiao F , Liu Y . 2015 . Overexpression of Arabidopsis XERICO gene confers enhanced drought and salt stress tolerance in rice (Oryza sativa L.) . Journal of Plant Biochemistry and Biotechnology 24 , 56 – 64 . Google Scholar CrossRef Search ADS Zeng W , Melotto M , He SY . 2010 . Plant stomata: a checkpoint of host immunity and pathogen virulence . Current Opinion in Biotechnology 21 , 599 – 603 . Google Scholar CrossRef Search ADS Zentella R , Zhang ZL , Park M et al. 2007 . Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis . The Plant Cell 19 , 3037 – 3057 . Google Scholar CrossRef Search ADS Zhang X , Zou Z , Gong P , Zhang J , Ziaf K , Li H , Xiao F , Ye Z . 2011 . Over-expression of microRNA169 confers enhanced drought tolerance to tomato . Biotechnology Letters 33 , 403 – 409 . Google Scholar CrossRef Search ADS Zhu Z , An F , Feng Y et al. 2011 . Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis . Proceedings of the National Academy of Sciences, USA 108 , 12539 – 12544 . Google Scholar CrossRef Search ADS © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: email@example.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
Journal of Experimental Botany – Oxford University Press
Published: Mar 17, 2018
It’s your single place to instantly
discover and read the research
that matters to you.
Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.
All for just $49/month
Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly
Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.
Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.
Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.
All the latest content is available, no embargo periods.
“Hi guys, I cannot tell you how much I love this resource. Incredible. I really believe you've hit the nail on the head with this site in regards to solving the research-purchase issue.”Daniel C.
“Whoa! It’s like Spotify but for academic articles.”@Phil_Robichaud
“I must say, @deepdyve is a fabulous solution to the independent researcher's problem of #access to #information.”@deepthiw
“My last article couldn't be possible without the platform @deepdyve that makes journal papers cheaper.”@JoseServera