To defend or to grow: lessons from Arabidopsis C24

To defend or to grow: lessons from Arabidopsis C24 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. 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To defend or to grow: lessons from Arabidopsis C24

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com
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0022-0957
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1460-2431
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10.1093/jxb/ery106
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Abstract

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. 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Journal of Experimental BotanyOxford University Press

Published: Mar 17, 2018

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