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

Abstract

Reproduction is a crucial process in the life span of flowering plants, and directly affects human basic requirements in agriculture, such as grain yield and quality. Typical receptor-like protein kinases (RLKs) are a large family of membrane proteins sensing extracellular signals to regulate plant growth, development, and stress responses. In Arabidopsis thaliana and other plant species, RLK-mediated signaling pathways play essential roles in regulating the reproductive process by sensing different ligand signals. Molecular understanding of the reproductive process is vital from the perspective of controlling male and female fertility. Here, we summarize the roles of RLKs during plant reproduction at the genetic and molecular levels, including RLK-mediated floral organ development, ovule and anther development, and embryogenesis. In addition, the possible molecular regulatory patterns of those RLKs with unrevealed mechanisms during reproductive development are discussed. We also point out the thought-provoking questions raised by the research on these plant RLKs during reproduction for future investigation.

Keywords: anther; embryo; floral meristem; ovule; receptor-like protein kinase; reproductive development.

Figure 1

RLKs regulate floral meristem identity and floral organ development. (A) Diagrams showing the process of flower development. At stage 3 (ST3), the sepal primordia begin to form at the edge of the meristem. At ST6, the petal primordia start to form; as the floral meristem terminates, the carpels begin to develop. At ST9, the floral organs in each whorl continue to develop. At ST14, the siliques elongate and the seeds begin to develop after pollination is completed. (B) RLKs regulate floral meristem and floral organ development. CLV1, CLV2-CRN, and RPK2 recruit CIKs to form receptor-co-receptor complexes that mediate the CLV3-WUS feedback loop signaling to control floral meristem size and termination, and floral organ number. BAM1/2 regulate floral meristem size. ERf members play a role in determining floral meristem size and floral organ morphology. ACR4 regulates sepal morphology. SUB is involved in petal and carpel development. HAE/HSL2 and SERKs form a receptor-co-receptor complex that perceives the IDA signal processed by SBTs to regulate the initiation of floral organ abscission via a MAPK cascade pathway. Putative ligands and co-receptor RLKs are shown in gray. Colored ovals in the extracellular domains of RLKs represent predicted LRR motifs, except ACR4, which is a CR4-L-RLK. FM, floral meristem; g, gynoecium; pe, petals; se, sepals; st, stamens.

Figure 2

RLK regulates anther development. (A) Diagrams showing the process of anther development. At ST2, the archesporial cells are formed at four corners of the anther. At ST3, the archesporial cells divide periclinally to produce the primary sporogenous cells and primary parietal cells. At ST4, the primary parietal cells divide to generate the inner and outer secondary parietal cells. At ST5, the inner secondary parietal cells divide to generate the middle layer and tapetum. At ST9, the middle layer degenerates and the pollen wall begins to develop. At ST12, mature pollen grains are formed and the endothecium is lignified and thickened. (B) RLKs regulate anther development. CLV1 and CLV2-CRN recruit CIKs to form the receptor-co-receptor complexes that may sense CLV3 to regulate anther morphogenesis and lobe development. ERf members function with MPK3/6 to regulate lobe development. The BAM1/2-CIK receptor-co-receptor complex determines archesporial cell division and differentiation. The RPK2-CIK receptor-co-receptor complex regulates archesporial cell division, primary parietal cell and inner secondary parietal cell division and differentiation, and anther dehiscence. The TPD1-EMS1-SERK1/2 signaling activates BES1 family transcription factors to determine tapetum identity and microspore mother cell development. BRI1 and SERKs mediate BR signaling to regulate the development of tapetum, microspores, and pollen. AtVRLK1 is involved in anther dehiscence. Colored ovals in the extracellular domains of RLKs represent predicted LRR motifs. Putative ligands and co-receptor RLKs are shown in gray. Ar, archesporial cell; E, epidermis; En, endothecium; ISP, inner secondary parietal cell; ML, middle layer; MMC, microspore mother cell; MSp, microspores; OSP, outer secondary parietal cell; PG, pollen grains; PP, primary parietal cell; PS, primary sporogenous cell; Sp, sporogenous cell; T, tapetum.

Figure 3

RLKs mediate ovule development. (A) Diagrams showing the process of ovule development. ST1-II is ovule primordium initiation and elongation. At ST2-III, the integument initiates to development. At ST2-V, the integument is stretched to the top of the nucellus. At ST3-VI, the ovule generates an embryo sac wrapped by the inner and outer integuments. (B) RLKs regulate ovule development. ERf members regulate initiation patterns of the ovule primordium and development of the integument and embryo sac. The BR signaling pathway is involved in the determination of ovule number and outer integument development. ACR4 regulates integument development. ALE2 controls integument and embryo sac development. SUB regulates outer integument development. Colored ovals in the extracellular domains of RLKs represent predicted LRR motifs except the CR4-L-RLK ACR4 and the extensin RLK ALE2. Putative ligands and co-receptor RLKs are shown in gray. es, embryo sac; i, integument; ii, inner integument; n, nucellus; oi, outer integument.

Figure 4

RLKs regulate embryo development. (A) Diagrams showing the process of embryo development, including the typical zygote, 1-cell, octant, dermatogen, globular, transition, hart, and torpedo stages. (B) RLKs regulate embryo development. ESF1, ERf-BSK1/2, SSP, and ZAR1 share the YDA-mediated signaling cascade to regulate zygote development. SERKs play a critical role in maintaining identity of the ground tissue stem cells through the YDA-MKK4/5 signaling pathway. RPK1 and TOAD2 maintain identity of radial pattern formation, and regulate hypophysis differentiation and cotyledon development. ACR4 and ALE2 function in the same process to regulate development of the protoderm and epidermis. The KRS peptide signal regulates formation of the embryo sheath formation. The GSO1/2-SERK receptor-co-receptor complex perceives the TWS1 peptide processed by ALE1 to control integrity of the embryonic cuticle via MPK6. ERf members play a role in cotyledon development. EXS regulates seed size. Colored ovals in the extracellular domains of RLKs represent predicted LRR motifs except the CR4-L-RLK ACR4 and the extensin RLK ALE2. Putative ligands, receptor RLKs, and co-receptor RLKs are shown in gray.