Cellular and transcriptomic analyses reveal two-staged chloroplast biogenesis underpinning photosynthesis build-up in the wheat leaf

Naresh Loudya,Enrique López-Juez,Laszlo Bogre,Priyanka Mishra,Yukiko Uehara-Yamaguchi,Kotaro Takahagi,Keiichi Mochida,Komaki Inoue

doi:10.1186/s13059-021-02366-3

Abstract

BackgroundThe developmental gradient in monocot leaves has been exploited to uncover leaf developmental gene expression programs and chloroplast biogenesis processes. However, the relationship between the two is barely understood, which limits the value of transcriptome data to understand the process of chloroplast development.ResultsTaking advantage of the developmental gradient in the bread wheat leaf, we provide a simultaneous quantitative analysis for the development of mesophyll cells and of chloroplasts as a cellular compartment. This allows us to generate the first biologically-informed gene expression map of this leaf, with the entire developmental gradient from meristematic to fully differentiated cells captured. We show that the first phase of plastid development begins with organelle proliferation, which extends well beyond cell proliferation, and continues with the establishment and then the build-up of the plastid genetic machinery. The second phase is marked by the development of photosynthetic chloroplasts which occupy the available cellular space. Using a network reconstruction algorithm, we predict that known chloroplast gene expression regulators are differentially involved across those developmental stages.ConclusionsOur analysis generates both the first wheat leaf transcriptional map and one of the most comprehensive descriptions to date of the developmental history of chloroplasts in higher plants. It reveals functionally distinct plastid and chloroplast development stages, identifies processes occurring in each of them, and highlights our very limited knowledge of the earliest drivers of plastid biogenesis, while providing a basis for their future identification.

Highlights

The developmental gradient in monocot leaves has been exploited to uncover leaf developmental gene expression programs and chloroplast biogenesis processes
Developmental analysis of the wheat leaf reveals stages of cell and chloroplast differentiation In order to generate a quantitative analysis of chloroplast biogenesis and a simultaneous global gene expression map of the developing wheat leaf, we first carried out a careful selection of biological material
Elegant measurements by Boffey et al [15], of the first leaf of wheat grown under conditions similar to ours, identified the relationship between distance from the leaf base and cellular age after exit from the shoot meristem

Summary

Introduction

The developmental gradient in monocot leaves has been exploited to uncover leaf developmental gene expression programs and chloroplast biogenesis processes. Rational engineering of photosynthetic performance could provide the best available avenue to increase crop yield potential [1]. For such an approach to be undertaken, a fundamental understanding of chloroplast development is an absolute prerequisite. Monocot leaves, where cell proliferation and differentiation are displayed along a linear developmental gradient, provide an ideally suited experimental system to study these processes. Leaf primordia form at the flanks of the stem cell population in the shoot apical meristem. Differentiation subsequently occurs in leaf primordia basipetally, resulting in a gradient of distinguishable cellular morphologies of distal differentiated cells towards the tip of the leaf, basal progenitor proliferating cells adjacent to the shoot apical meristem, and all possible intermediate stages in between

Methods

Results

Discussion

Conclusion