Constitutive signaling activity of a receptor-associated protein links fertilization with embryonic patterning in Arabidopsis thaliana

Abstract

In flowering plants, the asymmetrical division of the zygote is the first hallmark of apical-basal polarity of the embryo and is controlled by a MAP kinase pathway that includes the MAPKKK YODA (YDA). In Arabidopsis, YDA is activated by the membraneassociated pseudokinase SHORT SUSPENSOR (SSP) through an unusual parent-of-origin effect: SSP transcripts accumulate specifically in sperm cells but are translationally silent. Only after fertilization is SSP protein transiently produced in the zygote, presumably from paternally inherited transcripts. SSP is a recently diverged, Brassicaceae-specific member of the BRASSINOSTEROID SIGNALING KINASE (BSK) family. BSK proteins typically play broadly overlapping roles as receptorassociated signaling partners in various receptor kinase pathways involved in growth and innate immunity. This raises two questions: How did a protein with generic function involved in signal relay acquire the property of a signal-like patterning cue, and how is the early patterning process activated in plants outside the Brassicaceae family, where SSP orthologs are absent? Here, we show that Arabidopsis BSK1 and BSK2, two close paralogs of SSP that are conserved in flowering plants, are involved in several YDA-dependent signaling events, including embryogenesis. However, the contribution of SSP to YDA activation in the early embryo does not overlap with the contributions of BSK1 and BSK2. The loss of an intramolecular regulatory interaction enables SSP to constitutively activate the YDA signaling pathway, and thus initiates apical-basal patterning as soon as SSP protein is translated after fertilization and without the necessity of invoking canonical receptor activation.Arabidopsis thaliana | evolution | MAP kinase signaling | embryogenesis |

The short and intricate life of the suspensor

“…SSP transcripts are provided by the sperm cells and are translated in the zygote and endosperm where SSP binds to YDA (Yuan et al ). SSP has been found to bind to YODA‐dependent genes in vivo through its tetratricopeptide repeat (TPR) motif (Neu et al ). SSP is capable of constitutively activating YDA, but the structurally similar brassinosteriod signalling kinases (BSK) 1 and 2, which have also been shown to activate YDA, cannot (Neu et al ).…”

“…SSP has been found to bind to YODA‐dependent genes in vivo through its tetratricopeptide repeat (TPR) motif (Neu et al ). SSP is capable of constitutively activating YDA, but the structurally similar brassinosteriod signalling kinases (BSK) 1 and 2, which have also been shown to activate YDA, cannot (Neu et al ). This constitutive activation is likely due to the lack of an intramolecular interaction between the kinase domain and the TPR motif of SSP, differentiating it from the BSK proteins.…”

“…Mutations in the GRD gene yield similar phenotypes to YDA pathway mutants; however, GRD is not regulated by the YDA cascade pathway, indicating an indirect interaction (Jeong et al ). Neu et al () showed that a triple knockout of ssp and two related genes, bsk1 and bsk2 , resulted in a phenotype only slightly weaker than that of yda mutants.…”

Plasmogamic Paternal Contributions to Early Zygotic Development in Flowering Plants

“…Although the BSK family members, BSK1 and BSK2, cannot completely complement the loss of SSP, these may weakly activate the YDA-MAPK cascade in parallel to SSP (Neu et al, 2019). The bsk1;bsk2;ssp triple mutant phenotype, however, is still weaker than that of yda (Neu et al, 2019), indicating another signaling input for the full activation of YDA.…”

“…Premature stop (ssp-1) or null (ssp-2) mutations showed symmetric division and arrested cell elongation in the zygote; however, the ssp-2 phenotype in the Colombia-0 ecotype is much weaker than the ssp-1 phenotype and the yda phenotype in the Landsberg erecta ecotype ( Supplementary Table S1; Lukowitz et al, 2004;Bayer et al, 2009). Although the BSK family members, BSK1 and BSK2, cannot completely complement the loss of SSP, these may weakly activate the YDA-MAPK cascade in parallel to SSP (Neu et al, 2019). The bsk1;bsk2;ssp triple mutant phenotype, however, is still weaker than that of yda (Neu et al, 2019), indicating another signaling input for the full activation of YDA.…”