Mapping signaling networks and rapidly evolving genes in the developing Arabidopsis seed at single-nucleus resolution

Abstract

Seeds are an exceptional evolutionary innovation that enables the conditional allocation of maternal resources to successfully fertilized ovules. During early development, seeds accumulate nutrients that are utilized either by the embryo or by humans who harvest seed crops for food, biofuel, and livestock feed. Moreover, the grains of maize, rice, and wheat provide approximately 60% of the calories consumed worldwide. Although seeds are a cornerstone for ecosystems and modern agriculture, fundamental aspects of their development are incompletely understood. In this thesis, I develop a transcriptional atlas of seed development using the model plant Arabidopsis thaliana to clarify the functional compartmentalization, diversity, and developmental dynamics of cell types in the seed. I focus my analyses on how seed cell types communicate with one another to ensure successful propagation, and how genetic conflicts in the seed may drive rapid evolution in specific cell types. After characterizing the extent of short, secreted peptide expression in specific seed cell types, I perform in silico screens to match potential peptide hormones with their receptors. In total, I show that the seed coat shows functional compartmentalization around the gateway for maternal resources into seeds, that seed genes differentially expressed in a maternal resource transfer structure are rapidly evolving, and that genes underlying brassinosteroid biosynthesis and response are expressed in adjacent tissues, among other findings. This thesis illuminates potentially new mechanisms for inter-tissue coordination and provides a transcriptional reference for future seed studies.