Abstract

Cell walls, constructed by precisely choreographed changes in the plant secretome, play critical roles in plant cell physiology and development. Along with structural polysaccharides, secreted proline-rich Tandem Repeat Proteins (TRPs) are important for cell wall function, yet the evolutionary diversity of these structural TRPs remains virtually unexplored. Using a systems-level computational approach to analyze taxonomically diverse plant sequence data, we identified 31 distinct Pro-rich TRP classes targeted for secretion. This analysis expands upon the known phylogenetic diversity of extensins, the most widely studied class of wall structural proteins, and demonstrates that extensins evolved before plant vascularization. Our results also show that most Pro-rich TRP classes have unexpectedly restricted evolutionary distributions, revealing considerable differences in plant secretome signatures that define unexplored diversity.

Highlights

  • Composed primarily of polysaccharides, plant cell walls provide critical structural support for terrestrial plant life, and play important roles in plant growth, development, and interactions with microbes

  • Post-translationally modified from Pro-rich polypeptides, secreted HRGPs are generally grouped into three broad classes based on primary sequence architectures and glycosylation profiles [9,14,15,16], and these three classes, the extensin glycoproteins, the proline-rich proteins (PRPs), and the highly glycosylated arabinogalactan proteins (AGPs), have been hypothesized to form a phylogenetic continuum ranging from green algae throughout land plants [9,17]

  • To explore the global diversity of Pro-rich Tandem Repeat Proteins (TRPs), we constructed a database containing 8.3 M full and partial protein sequences, from genome and EST projects, spanning 36,815 plant and green algal species

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Summary

Introduction

Plant cell walls provide critical structural support for terrestrial plant life, and play important roles in plant growth, development, and interactions with microbes. Ubiquitous in green plants, Hyp-rich glycoproteins, commonly known as HRGPs or extensins [8,9], compose up to 10% of the cell wall mass of higher plants [6,7], and have been shown to play critical roles in cell wall structure and function [10,11,12,13]. Post-translationally modified from Pro-rich polypeptides, secreted HRGPs are generally grouped into three broad classes based on primary sequence architectures and glycosylation profiles [9,14,15,16], and these three classes, the extensin glycoproteins, the proline-rich proteins (PRPs), and the highly glycosylated arabinogalactan proteins (AGPs), have been hypothesized to form a phylogenetic continuum ranging from green algae throughout land plants [9,17]

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