BZR1 Transcription Factor Regulates Heat Stress Tolerance Through FERONIA Receptor-Like Kinase-Mediated Reactive Oxygen Species Signaling in Tomato

Yin, Yanling; Qin, Kezhen; Song, Xuchen; Zhang, Qihao; Zhou, Yanhong; Xia, Xiaojian; Yu, Jingquan

doi:10.1093/pcp/pcy146

Cited by 97 publications

(81 citation statements)

References 70 publications

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“…Besides, FER was initially identified from a pollen tube reception mutant (Huck et al , ; Rotman et al , ; Escobar‐Restrepo et al , ), and was further demonstrated as an essential regulator of hormone response and cell growth regulation (Lindner et al , ; Li et al , ). Recently, we have discovered that BZR1 regulates thermotolerance through ROS signaling mediated by FERNOIA receptor‐like kinases FER2 and FER3 in tomato (Yin et al , ). Furthermore, we have assessed the pollen fertility of the CRISPR‐ fer2 and CRISPR‐ fer3 mutants and found that pollen viability, pollen germination rate and mature pollen morphology were significantly deficient compared with WT plants (Figure S15).…”

Section: Discussionmentioning

confidence: 99%

Brassinosteroid‐mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

et al. 2020

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Phytohormone brassinosteroids (BRs) are essential for plant growth and development, but the mechanisms of BR-mediated pollen development remain largely unknown. In this study, we show that pollen viability, pollen germination and seed number decreased in the BR-deficient mutant d^i m , which has a lesion in the BR biosynthetic gene DWARF (DWF), and in the bzr1 mutant, which is deficient in BR signaling regulator BRASSINAZOLE RESISTANT 1 (BZR1), compared with those in wild-type plants, whereas plants overexpressing DWF or BZR1 exhibited the opposite effects. Loss or gain of function in the DWF or BZR1 genes altered the timing of reactive oxygen species (ROS) production and programmed cell death (PCD) in tapetal cells, resulting in delayed or premature tapetal degeneration, respectively. Further analysis revealed that BZR1 could directly bind to the promoter of RESPIRATORY BURST OXIDASE HOMOLOG 1 (RBOH1), and that RBOH1-mediated ROS promote pollen and seed development by triggering PCD and tapetal cell degradation. In contrast, the suppression of RBOH1 compromised BR signaling-mediated ROS production and pollen development. These findings provide strong evidence that BZR1-dependent ROS production plays a critical role in the BR-mediated regulation of tapetal cell degeneration and pollen development in Solanum lycopersicum (tomato) plants.

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Section: Discussionmentioning

confidence: 99%

Brassinosteroid‐mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

et al. 2020

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“…The BES1/BZR1s are a large family of plant-specific transcription factors that are involved in plant growth and developmental processes, autophagy as well as response to nitrogen starvation [18,19,38]. Some prior studies have shown that the BES1/BZR1 genes are regulated by drought, salt, cold and heat stress in Brassica rapa, Eucalyptus grandis, Brassica napus and Arabidopsis [44][45][46], and accelerate drought, heat and freezing tolerance in tomato or Arabidopsis [32][33][34][35], implying that BES1/BZR1 genes participate in the osmotic stress response. In our study, the ZmBES1/BZR1-5 gene also responds to salt and drought stress in maize (Figure 1), which may be related to the cis-acting elements of its promoter [23].…”

Section: Discussionmentioning

confidence: 99%

“…Likewise, BES1/BZR1s control cell and hypocotyl elongation by interacting with the light signal regulators PIF4, PhyB, UVB8 and CRY1 [20,[28][29][30]. Recently, BES1/BZR1s have been reported to regulate drought, heat and freezing stress response through regulating the expression of glutathione S-transferase 1 (GST1), RESPONSIVE TO DESICCATION 26 (RD26) and CBF genes, as well as interacting with RD26 and WRKY transcription factors [31][32][33][34][35]. In addition to their crucial roles in abiotic stress, BES1/BZR1s also function in response to biotic and nutrition stresses, such as immunity, autophagy, nitrogen and phosphorus starvation [36][37][38].…”

Section: Introductionmentioning

confidence: 99%

Maize ZmBES1/BZR1-5 Decreases ABA Sensitivity and Confers Tolerance to Osmotic Stress in Transgenic Arabidopsis

Sun

et al. 2020

IJMS

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The BRI1-EMS suppressor 1 (BES1)/brassinazole-resistant 1 (BZR1) transcription factors, key components in the brassinosteroid signaling pathway, play pivotal roles in plant growth and development. However, the function of BES1/BZR1 in crops during stress response remains poorly understood. In the present study, we characterized ZmBES1/BZR1-5 from maize, which was localized to the nucleus and was responsive to abscisic acid (ABA), salt and drought stresses. Heterologous expression of ZmBES1/BZR1-5 in transgenic Arabidopsis resulted in decreased ABA sensitivity, facilitated shoot growth and root development, and enhanced salt and drought tolerance with lower malondialdehyde (MDA) content and relative electrolyte leakage (REL) under osmotic stress. The RNA sequencing (RNA-seq) analysis revealed that 84 common differentially expressed genes (DEGs) were regulated by ZmBES1/BZR1-5 in transgenic Arabidopsis. Subsequently, gene ontology and KEGG pathway enrichment analyses showed that the DEGs were enriched in response to stress, secondary metabolism and metabolic pathways. Furthermore, 30 DEGs were assigned to stress response and possessed 2–15 E-box elements in their promoters, which could be potentially recognized and bound by ZmBES1/BZR1-5. Taken together, our results reveal that the ZmBES1/BZR1-5 transcription factor positively regulates salt and drought tolerance by binding to E-box to induce the expression of downstream stress-related genes. Therefore, our study contributes to the better understanding of BES1/BZR1 function in the stress response of plants.

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“…Studies on BR signalling mutants of Arabidopsis , tomato and other crops revealed that BRs play a protective role under high temperature, as they promote antioxidant enzyme activities and elevate RBOH1 transcription [ 27 , 32 ]. In tomato, overexpression of BZR1 enhanced the transcription of RBOH1 and subsequently elevated heat tolerance, and seedling of the SlBRI1 mutant cu3 -abs1 exhibited induction of thermotolerance, showing increased signs of oxidative stress [ 29 , 33 ]. In this study, P SlBRI1 ::S1040A-GFP lines that were tolerant to heat stress showed higher expression levels of RBOH1 but lower accumulation of H 2 O 2 than P SlBRI1 ::S1040D-GFP and P SlBRI1 ::SlBRI1-GFP plants after heat stress ( Figure 6 and Figure 8 ).…”

Section: Discussionmentioning

confidence: 99%

Modification of Serine 1040 of SIBRI1 Increases Fruit Yield by Enhancing Tolerance to Heat Stress in Tomato

Wang

Tian

et al. 2020

IJMS

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High temperature is a major environmental factor that adversely affects plant growth and production. SlBRI1 is a critical receptor in brassinosteroid signalling, and its phosphorylation sites have differential functions in plant growth and development. However, the roles of the phosphorylation sites of SIBRI1 in stress tolerance are unknown. In this study, we investigated the biological functions of the phosphorylation site serine 1040 (Ser-1040) of SlBRI1 in tomato. Phenotype analysis indicated that transgenic tomato harbouring SlBRI1 dephosphorylated at Ser-1040 showed increased tolerance to heat stress, exhibiting better plant growth and plant yield under high temperature than transgenic lines expressing SlBRI1 or SlBRI1 phosphorylated at Ser-1040. Biochemical and physiological analyses further showed that antioxidant activity, cell membrane integrity, osmo-protectant accumulation, photosynthesis and transcript levels of heat stress defence genes were all elevated in tomato plants harbouring SlBRI1 dephosphorylated at Ser-1040, and the autophosphorylation level of SlBRI1 was inhibited when SlBRI1 dephosphorylated at Ser-1040. Taken together, our results demonstrate that the phosphorylation site Ser-1040 of SlBRI1 affects heat tolerance, leading to improved plant growth and yield under high-temperature conditions. Our results also indicate the promise of phosphorylation site modification as an approach for protecting crop yields from high-temperature stress.

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BZR1 Transcription Factor Regulates Heat Stress Tolerance Through FERONIA Receptor-Like Kinase-Mediated Reactive Oxygen Species Signaling in Tomato

Cited by 97 publications

References 70 publications

Brassinosteroid‐mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

Brassinosteroid‐mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

Maize ZmBES1/BZR1-5 Decreases ABA Sensitivity and Confers Tolerance to Osmotic Stress in Transgenic Arabidopsis

Modification of Serine 1040 of SIBRI1 Increases Fruit Yield by Enhancing Tolerance to Heat Stress in Tomato

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