FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa

Zhang, Lili; Huang, Jiabao; Su, Shiqi; Wei, Xiaochun; Yang, Lin; Zhao, Huanhuan; Yu, Jian‐Qiang; Wang, Jie; Hui, Jiyun; Hao, Shiya; Song, Shanshan; Cao, Yanyan; Wang, Maoshuai; Zhang, Xiaowei; Zhao, Yanyan; Wang, Zhiyong; Zeng, Weiqing; Wu, Hen-Ming; Yuan, Yuxiang; Zhang, Xiansheng; Cheung, Alice Y.; Duan, Qiaohong

doi:10.1016/j.cub.2021.04.060

Cited by 89 publications

(89 citation statements)

References 103 publications

(161 reference statements)

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“…It will now be essential to elucidate the downstream mechanism or mechanisms that block the emergence of secondary pollen tubes at the septum. Further components of this polytubey block may include nitric oxide ( 11 ); secretion of cell wall components; and ROS that mediate FER-controlled pollen tube rupture ( 21 ), pollen hydration ( 31 ), and self-incompatibility ( 32 ).…”

Section: Discussionmentioning

confidence: 99%

RALF peptide signaling controls the polytubey block in Arabidopsis

Zhong

Wang

et al. 2022

Science

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Fertilization of an egg by multiple sperm (polyspermy) leads to lethal genome imbalance and chromosome segregation defects. In Arabidopsis thaliana , the block to polyspermy is facilitated by a mechanism that prevents polytubey (the arrival of multiple pollen tubes to one ovule). We show here that FERONIA, ANJEA, and HERCULES RECEPTOR KINASE 1 receptor-like kinases located at the septum interact with pollen tube–specific RALF6, 7, 16, 36, and 37 peptide ligands to establish this polytubey block. The same combination of RALF (rapid alkalinization factor) peptides and receptor complexes controls pollen tube reception and rupture inside the targeted ovule. Pollen tube rupture releases the polytubey block at the septum, which allows the emergence of secondary pollen tubes upon fertilization failure. Thus, orchestrated steps in the fertilization process in Arabidopsis are coordinated by the same signaling components to guarantee and optimize reproductive success.

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Section: Discussionmentioning

confidence: 99%

RALF peptide signaling controls the polytubey block in Arabidopsis

Zhong

Wang

et al. 2022

Science

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“…In the ROS and •OH measurement assays, fresh anthers of WT and ms33-6038 at different developmental stages were immersed in a 2 mL centrifuge tube, which contained 1 mL of 1× HHBS. After washing the anthers, the supernatant was discarded, a 1 mL working solution (1 mL of H 2 DCF-DA for ROS measurement or 1 mL of HPF working solution for •OH measurement) and 0.5 μL of Silwet L-77 (SL77080596, GE, Boston, MA, USA) was added; it was vacuumed for 15 min and then shaken at 25 °C in darkness (80–100 rmp) for 3 h. After discarding the dye solution, anthers were washed once with 1× HHBS, then 1 mL of 1× HHBS was added into the centrifuge tube [ 40 , 41 ]. The green fluorescence signals were detected by a Leica TCS SP8 confocal microscope (Leica, Wetzlar, Germany).…”

Section: Methodsmentioning

confidence: 99%

The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers

Liu

Zhu

et al. 2022

Cells

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In plants, oxidative stress and metabolic reprogramming frequently induce male sterility, however our knowledge of the underlying molecular mechanism is far from complete. Here, a maize genic male-sterility (GMS) mutant (ms33-6038) with a loss-of-function of the ZmMs33 gene encoding glycerol-3-phosphate acyltransferase 6 (GPAT6) displayed severe deficiencies in the development of a four-layer anther wall and microspores and excessive reactive oxygen species (ROS) content in anthers. In ms33-6038 anthers, transcriptome analysis identified thousands of differentially expressed genes that were functionally enriched in stress response and primary metabolism pathways. Further investigation revealed that 64 genes involved in ROS production, scavenging, and signaling were specifically changed in expression levels in ms33-6038 anthers compared to the other five investigated GMS lines. The severe oxidative stress triggered premature tapetal autophagy and metabolic reprogramming mediated mainly by the activated SnRK1-bZIP pathway, as well as the TOR and PP2AC pathways, proven by transcriptome analysis. Furthermore, 20 reported maize GMS genes were altered in expression levels in ms33-6038 anthers. The excessive oxidative stress and the metabolic reprogramming resulted in severe phenotypic deficiencies in ms33-6038 anthers. These findings enrich our understanding of the molecular mechanisms by which ROS and metabolic homeostasis impair anther and pollen development in plants.

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“…Furthermore, GRMZM2G006080, which encodes a FER receptor‐like protein kinase in maize ( Zea mays ), is a candidate gene responsible for a quantitative trait locus (QTL) associated with the control of kernel size (Wang et al ., 2020b). In Chinese cabbage ( Brassica rapa ), FER homologues affect pollen–stigma interactions by controlling ROS production (Zhang et al ., 2021).…”

Section: Beyond Arabidopsis: Roles Of Crrlk1ls In Other Plant Lineagesmentioning

confidence: 99%

New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signalling network

Zhu

et al. 2021

New Phytologist

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Receptor-like kinases (RLKs), which constitute the largest receptor family in plants, are essential for perceiving and relaying information about various environmental stimuli. Tremendous progress has been made in the past few decades towards elucidating the mechanisms of action of several RLKs, with emerging paradigms pointing to their roles in cell adaptations. Among these paradigms, Catharanthus roseus receptor-like kinase 1-like (CrRLK1L) proteins and their rapid alkalinization factor (RALF) peptide ligands have attracted much interest. In particular, FERONIA (FER) is a CrRLK1L protein that participates in a wide array of physiological processes associated with RALF signalling, including cell growth and monitoring cell wall integrity, RNA and energy metabolism, and phytohormone and stress responses. Here, we analyse FER in the context of CrRLK1L members and their ligands in multiple species. The FER working model raises many questions about the role of CrRLK1L signalling networks during cell adaptation. For example, how do CrRLK1Ls recognize various RALF peptides from different organisms to initiate specific phosphorylation signal cascades? How do RALF-FER complexes achieve their specific, sometimes opposite, functions in different cell types? Here, we summarize recent major findings and highlight future perspectives in the field of CrRLK1L signalling networks.

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FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa

Cited by 89 publications

References 103 publications

RALF peptide signaling controls the polytubey block in Arabidopsis

RALF peptide signaling controls the polytubey block in Arabidopsis

The Loss-Function of the Male Sterile Gene ZmMs33/ZmGPAT6 Results in Severely Oxidative Stress and Metabolic Disorder in Maize Anthers

New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signalling network

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