SERKs regulate embryonic cuticle integrity through the TWS1‐GSO1/2 signaling pathway in Arabidopsis

Abstract

The embryonic cuticle integrity is critical for the embryo to separate from the neighboring endosperm. The sulfated TWISTED SEED1 (TWS1) peptide precursor generated in the embryo diffuses through gaps of the nascent cuticle to the surrounding endosperm, where it is cleaved by ABNORMAL LEAF SHAPE1 (ALE1) and becomes an active mature form. The active TWS1 is perceived by receptor-like protein kinases GASSHO1 (GSO1) and GSO2 in the embryonic epidermal cells to start the downstream signaling and guide the formation of an intact embryonic cuticle. However, the early signaling events after TWS1 is perceived by GSO1/2 are still unknown.Here, we report that serk1/2/3 embryos show cuticle defects similar to ale1, tws1, and gso1/2. Genetic and biochemical analyses were performed to dissect the signaling pathway mediated by SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASEs (SERKs) during cuticle development.SERKs function with GSO1/2 in a common pathway to monitor the integrity of the embryonic cuticle. SERKs interact with GSO1/2, which can be enhanced dramatically by TWS1. The phosphorylation levels of SERKs and GSO1/2 rely on each other and can respond to and be elevated by TWS1.Our results demonstrate that SERKs may function as coreceptors of GSO1/2 to transduce the TWS1 signal and ultimately regulate embryonic cuticle integrity.

Receptor-like protein kinases in plant reproduction: Current understanding and future perspectives

“…Exogenously applied TWS1 peptide can enhance the interaction between GSO1/2 and SERKs, and the phosphorylation levels of GSO1/2 and SERKs. Moreover, the phosphorylation enhancement of SERKs in response to TWS1 is dependent on GSO1/2 ( Zhang et al, 2022 ). Therefore, SERKs are recruited by GSO1/2 to form a receptor-co-receptor complex that recognizes TWS1 and regulates embryonic cuticle development.…”

“…In the past two decades, studies have shown that many RLKs play essential roles to regulate orchestrated development of reproductive organs by mediating a variety of ligand signals, and several important achievements were made. For example, the TPD1-EMS1-SERK1/2 signaling in tapetum specification, TWS1-GSO1/2-SERK signaling in embryonic cuticle formation, and the HAE/HSL2-SERK complex-mediated IDA signaling in the floral organ abscission process have been largely clarified ( Li et al., 2017 ; Jia et al., 2008 ; Cho et al., 2008 ; Meng et al., 2016 ; Santiago et al., 2016 ; Doll et al., 2020 ; Zhang et al., 2022 ) ( Figures 1 B, 2 B, and 4 B; Table 1 ). Furthermore, CIKs from the same LRR II-RLK family have been recently identified to be novel co-receptors that play crucial roles in meristem maintenance and anther cell specification ( Cui et al., 2018 ; Hu et al., 2018 ; Gou and Li, 2020 ) ( Figure 2 B; Table 1 ).…”

“…It is common that one RLK or members from the same RLK subfamily are employed to regulate different biological processes during reproductive development, suggesting that similar strategies involved in RLK signaling may be recruited by different development processes during evolution. For instance, SERKs play key functions in regulating tapetum specification, floral organ abscission, embryonic stem cell maintenance, and embryonic cuticle integrity ( Meng et al., 2016 ; Li et al., 2017 , 2019 ; Zhang et al., 2022 ) ( Figures 1 B, 2 B, and 4 B; Table 1 ). The CLV3-CLV1-CIK signaling pathway not only regulates the floral meristem size but also controls the lobe development ( Cui et al., 2018 ; Hu et al., 2018 ) ( Figures 1 B and 2 B; Table 1 ).…”

“…For example, EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS (EMS1/EXS) functions together with SERK1/2 to sense the microspore mother cell-originated small peptide TAPETUM DETERMINANT 1 (TPD1), which determines the differentiation of the tapetum by activating the downstream core transcription factor BRI1 EMS SUPPRESSOR 1 (BES1) and its homologues ( Yin et al., 2002 ; Jia et al., 2008 ; Li et al., 2017 ; Chen et al., 2019 ; Zheng et al., 2019 ). During embryogenesis, GASSHO 1 (GSO1) and GSO2 function with SERKs to perceive the endosperm-processed TWISTED SEED 1 (TWS1) signal, mediating the communications between the embryo and the endosperm to control the cuticle integrity in embryonic epidermal cells ( Tsuwamoto et al., 2008 ; Fiume et al., 2016 ; Doll et al., 2020 ; Zhang et al, 2022 ). In addition, it was revealed that POLLEN-SPECIFIC RECEPTOR KINASE 3/6 (PRK3/6), MALE DISCOVERER 1 (MDIS1), and MDIS1-INTERACTING RLK 1 (MIK1) play important roles to guide pollen tube growth by sensing the LURE signals during fertilization in Arabidopsis ( Takeuchi and Higashiyama, 2016 ; Wang et al., 2016 ; Zhang et al., 2017b ).…”

Arabidopsis ROOT ELONGATION RECEPTOR KINASES negatively regulate root growth putatively via altering cell wall remodeling gene expression

“…GASSHO 1 (GSO1) and GSO2 were initially identified to regulate the development of epidermal surface in Arabidopsis embryos (Tsuwamoto et al, 2008). Later they were determined as the receptors of peptide hormones TWISTED SEED and CASPARIAN STRIP INTEGRITY FACTOR 1 to mediate embryonic cuticle integrity and Casparian strip formation, respectively (Nakayama et al, 2017; Doll et al, 2020; Zhang et al, 2022). PEP1 RECEPTOR 1 (PEPR1) and PEPR2 are the receptors of an endogenous peptide PEP1 and play a role in innate immunity responses (Yamaguchi et al, 2006).…”