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

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 <i>Arabidopsis</i>, YDA is activated by the membrane-associated pseudokinase SHORT SUSPENSOR (SSP) through an unusual parent-of-origin effect: <i>SSP</i> 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. <i>SSP</i> is a recently diverged, Brassicaceae-specific member of the <i>BRASSINOSTEROID SIGNALING KINASE</i> (<i>BSK</i>) family. BSK proteins typically play broadly overlapping roles as receptor-associated 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 <i>SSP</i> orthologs are absent? Here, we show that <i>Arabidopsis BSK1</i> and <i>BSK2</i>, two close paralogs of <i>SSP</i> 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.