Plant Physiology

Li, Qianqian; Zhang, Xingli; Li, Haiyun; Zhang, Huihui; Hao, Hongyan; Yu, Wenjie; Sun, Jinbian; Fan, Yinglun; Lyu, Shanhua

doi: 10.1093/plphys/kiae585pmid: 39484976

An improved Agrobacterium tumefaciens–mediated genetic transformation protocol shortens the growth period by ∼6 to 9 wk.

Dao, Ousmane; Burlacot, Adrien; Buchert, Felix; Bertrand, Marie; Auroy, Pascaline; Stoffel, Carolyne; Madireddi, Sai Kiran; Irby, Jacob; Hippler, Michael; Peltier, Gilles; Li-Beisson, Yonghua

doi: 10.1093/plphys/kiae617

Waghmare, Sakharam; Xia, Lingfeng; Ly, Thu Phan; Xu, Jing; Farami, Sahar; Burchmore, Richard; Blatt, Michael R; Karnik, Rucha

doi: 10.1093/plphys/kiae541pmid: 39387490

Secretory trafficking in plant cells is facilitated by SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) proteins that drive membrane fusion of cargo-containing vesicles. In Arabidopsis, SYNTAXIN OF PLANTS 132 (SYP132) is an evolutionarily ancient SNARE that functions with syntaxins SYP121 and SYP122 at the plasma membrane. Whereas SYP121 and SYP122 mediate overlapping secretory pathways, albeit with differences in their importance in plant–environment interactions, the SNARE SYP132 is absolutely essential for plant development and survival. SYP132 promotes endocytic traffic of the plasma membrane H+-ATPase AHA1 and aquaporin PIP2;1, and it coordinates plant growth and bacterial pathogen immunity through PATHOGENESIS-RELATED1 (PR1) secretion. Yet, little else is known about SYP132 cargoes. Here, we used advanced quantitative tandem mass tagging (TMT)-MS combined with immunoblot assays to track native secreted cargo proteins in the leaf apoplast. We found that SYP132 supports a basal level of secretion in Arabidopsis leaves, and its overexpression influences salicylic acid and jasmonic acid defense-related cargoes including PR1, PR2, and PR5 proteins. Impairing SYP132 function also suppressed defense-related secretory traffic when challenged with the bacterial pathogen Pseudomonas syringae. Thus, we conclude that, in addition to its role in hormone-related H+-ATPase cycling, SYP132 influences basal plant immunity.

Yu, Xiao-Qian; Niu, Hao-Qiang; Zhang, Yue-Mei; Shan, Xiao-Xu; Liu, Chao; Wang, Hou-Ling; Yin, Weilun; Xia, Xinli

doi: 10.1093/plphys/kiae593pmid: 39503258

Enhanced autoimmunity often leads to impaired plant growth and development, and the coordination of immunity and growth in Populus remains elusive. In this study, we have identified the transcription factors PagWRKY33a/b as key regulators of immune response and growth maintenance in Populus. The disruption of PagWRKY33a/b causes growth issues and autoimmunity while conferring resistance to anthracnose caused by Colletotrichum gloeosporioides. PagWRKY33a/b binds to the promoters of N requirement gene 1.1 (NRG1.1) and Gibberellic Acid-Stimulated in Arabidopsis (GASA14) during infection, activating their transcription. This process maintains disease resistance and engages in GA signaling to reduce growth costs from immune activation. The oxPagWRKY33a/nrg1.1 mutant results in reduced resistance to C. gloeosporioides. Further, PagWRKY33a/b is phosphorylated and activated by mitogen-activated protein kinase kinase 1, which inhibits respiratory burst oxidase homolog D (RBOHD) and respiratory burst oxidase homolog I (RBOHI) transcription, causing reactive oxygen species bursts in wrky33a/b double mutants. This leads to an upregulation of PagNRG1.1 in the absence of pathogens. However, the wrky33a/b/nrg1.1 and wrky33a/b/rbohd triple mutants show compromised defense responses, underscoring the complexity of WRKY33 regulation. Additionally, the stability of PagWRKY33 is modulated by Ring Finger Protein 5 (PagRNF5)-mediated ubiquitination, balancing plant immunity and growth. Together, our results provide key insights into the complex function of WRKY33 in Populus autoimmunity and its impact on growth and development.

Sun, Yaqi; Sheng, Yuewen; Ni, Tao; Ge, Xingwu; Sarsby, Joscelyn; Brownridge, Philip J; Li, Kang; Hardenbrook, Nathan; Dykes, Gregory F; Rockliffe, Nichola; Eyers, Claire E; Zhang, Peijun; Liu, Lu-Ning

doi: 10.1093/plphys/kiae665pmid: 39680612

Carboxysomes are anabolic bacterial microcompartments that play an essential role in CO2 fixation in cyanobacteria. This self-assembling proteinaceous organelle uses a polyhedral shell constructed by hundreds of shell protein paralogs to encapsulate the key CO2-fixing enzymes Rubisco and carbonic anhydrase. Deciphering the precise arrangement and structural organization of Rubisco enzymes within carboxysomes is crucial for understanding carboxysome formation and overall functionality. Here, we employed cryoelectron tomography and subtomogram averaging to delineate the 3D packaging of Rubiscos within β-carboxysomes in the freshwater cyanobacterium Synechococcus elongatus PCC7942 grown under low light. Our results revealed that Rubiscos are arranged in multiple concentric layers parallel to the shell within the β-carboxysome lumen. We also detected Rubisco binding with the scaffolding protein CcmM in β-carboxysomes, which is instrumental for Rubisco encapsulation and β-carboxysome assembly. Using Quantification conCATamer-based quantitative MS, we determined the absolute stoichiometric composition of the entire β-carboxysome. This study provides insights into the assembly principles and structural variation of β-carboxysomes, which will aid in the rational design and repurposing of carboxysome nanostructures for diverse bioengineering applications.

Rolletschek, Hardy; Borisjuk, Ljudmilla; Gómez-Álvarez, Eva María; Pucciariello, Chiara

doi: 10.1093/plphys/kiae556pmid: 39471319

Seeds represent essential stages of the plant life cycle: embryogenesis, the intermittent quiescence phase, and germination. Each stage has its own physiological requirements, genetic program, and environmental challenges. Consequently, the effects of developmental and environmental hypoxia can vary from detrimental to beneficial. Past and recent evidence shows how low-oxygen signaling and metabolic adaptations to hypoxia affect seed development and germination. Here, we review the recent literature on seed biology in relation to hypoxia research and present our perspective on key challenges and opportunities for future investigations.

Blackman, Chris J; Halliwell, Ben; Brodribb, Tim J

doi: 10.1093/plphys/kiae632pmid: 39673329

The negative impacts of drought on plant productivity and survival in natural and crop systems are increasing with global heating, yet our capacity to identify species capable of surviving drought remains limited. Here, we tested the use of a mixed-planting approach for assessing differences in seedling drought tolerance. To homogenize dehydration rates, we grew seedlings of 10 species of Eucalyptus together in trays where roots of all individuals were overlapping in a common loam soil. These seedling combinations were dried down under cool and warm temperature conditions, and seedling responses were quantified from measurements of chlorophyll fluorescence (Fv/Fm). The day of drought (T) associated with an 88% decline in Fv/Fm (TF88) varied significantly among species and was unrelated to seedling size. No significant differences in water potentials were detected among seedlings dehydrated under warm conditions prior to leaf wilt. The rank-order of species TF88 was consistent under both temperature treatments. Under cool conditions, seedling TF88 increased with decreasing cavitation vulnerability measured on adult foliage. Under both treatments, a quadratic function best fit the relationship between seedling TF88 and sampling site mean annual precipitation. These results provide evidence for adaptive selection of seedling drought tolerance. Our findings highlight the use of mixed-planting experiments for comparing seedling drought tolerance with applications for improving plant breeding and conservation outcomes.

Huang, Li-Chao; Li, Yu-Yu; Lai, Jian-Xin; An, Yi; Song, Xue-Qin; Zhao, Shu-Tang; Zhang, Jin; Lu, Meng-Zhu

doi: 10.1093/plphys/kiae672pmid: 39715459

Tension wood (TW), characterized by increased cambium cell proliferation and few vessels, is a classical model for the mechanical analysis of wood formation. In this study, we found higher superoxide anion (O2.−) levels in the cambium zone of poplar (Populus alba × P. glandulosa clone “84K”) TW than in that of opposite wood during gravistimulation. Treatment with an O2.− activator (methyl viologen) resulted in tension-wood-like xylem tissue formation, and transgenic plants with reduced cambium O2.− levels presented an attenuated gravity response. Time-course detection of O2.− and indole-3-acetic acid (IAA) levels revealed that auxin responses were enhanced following increases in O2.− levels, suggesting that IAA mediates TW induction downstream of O2.−. Rapid division but advanced programmed cell death in cambium cells was detected in both gravistimulated and O2.− activator-treated plants. These findings suggest that high O2.− levels trigger downstream IAA signaling to promote cambium cell proliferation and induce TW formation.

Renziehausen, Tilo; Chaudhury, Rim; Hartman, Sjon; Mustroph, Angelika; Schmidt-Schippers, Romy R

doi: 10.1093/plphys/kiae596pmid: 39530170

Oxygen deficiency (hypoxia) occurs naturally in many developing plant tissues but can become a major threat during acute flooding stress. Consequently, plants as aerobic organisms must rapidly acclimate to hypoxia and the associated energy crisis to ensure cellular and ultimately organismal survival. In plants, oxygen sensing is tightly linked with oxygen-controlled protein stability of group VII ETHYLENE-RESPONSE FACTORs (ERFVII), which, when stabilized under hypoxia, act as key transcriptional regulators of hypoxia-responsive genes (HRGs). Multiple signaling pathways feed into hypoxia signaling to fine-tune cellular decision-making under stress. First, ATP shortage upon hypoxia directly affects the energy status and adjusts anaerobic metabolism. Secondly, altered redox homeostasis leads to reactive oxygen and nitrogen species (ROS and RNS) accumulation, evoking signaling and oxidative stress acclimation. Finally, the phytohormone ethylene promotes hypoxia signaling to improve acute stress acclimation, while hypoxia signaling in turn can alter ethylene, auxin, abscisic acid, salicylic acid, and jasmonate signaling to guide development and stress responses. In this Update, we summarize the current knowledge on how energy, redox, and hormone signaling pathways are induced under hypoxia and subsequently integrated at the molecular level to ensure stress-tailored cellular responses. We show that some HRGs are responsive to changes in redox, energy, and ethylene independently of the oxygen status, and we propose an updated HRG list that is more representative for hypoxia marker gene expression. We discuss the synergistic effects of hypoxia, energy, redox, and hormone signaling and their phenotypic consequences in the context of both environmental and developmental hypoxia.

Deng, Miaomiao; Zhang, Lei; Yang, Chao; Zeng, Qian; Zhong, Linlin; Guo, Xiaoli

doi: 10.1093/plphys/kiae548pmid: 39575886

Low oxygen availability within plant cells arises during plant development but is exacerbated under environmental stress conditions. The group VII ETHYLENE RESPONSE FACTOR (ERFVII) transcription factors have been identified as pivotal regulators in the hypoxia response to abiotic stress. However, their roles in transcriptional regulation during biotic stresses remain less defined. In this study, we investigated the biological function and regulatory mechanism of soybean (Glycine max) ERFVII transcription factors during soybean cyst nematode (Heterodera glycines Ichinohe) infection. We provide evidence that soybean cyst nematode infection induces responses at the infection sites similar to those induced by hypoxia, characterized by the stabilization of ERFVII proteins and increased expression of hypoxia-responsive genes. Hypoxia pretreatment of soybeans enhances their resistance to nematode infection. We demonstrate that ERFVII members GmRAP2.12 and GmRAP2.3 act as transcriptional activators to drive the expression of GmPR10-09g, a member of the PR10 gene family highly induced by soybean cyst nematode and positively impacting nematode resistance. Transgenic hairy root analysis of nematode infection for either GmRAP2.12 or N-end rule pathway components (GmATE or GmPRT6) indicates a positive role of ERFVIIs in soybean defense responses against cyst nematode. The results of our study emphasize the important functions of GmERFVIIs in strengthening soybean’s immune responses against cyst nematode by transcriptional activation of GmPR10.