Cell Wall Invertase Is Essential for Ovule Development through Sugar Signaling Rather Than Provision of Carbon Nutrients.

Shengjin Liao,Lu Wang,Jun Li,Yong-Ling Ruan

doi:10.1104/pp.20.00400

Abstract

Ovule formation is essential for realizing crop yield because it determines seed number. The underlying molecular mechanism, however, remains elusive. Here, we show that cell wall invertase (CWIN) functions as a positive regulator of ovule initiation in Arabidopsis (Arabidopsis thaliana). In situ hybridization revealed that CWIN2 and CWIN4 were expressed at the placenta region where ovule primordia initiated. Specific silencing of CWIN2 and CWIN4 using targeted artificial microRNA driven by an ovule-specific SEEDSTICK promoter (pSTK) resulted in a substantial reduction of CWIN transcript and activity, which blocked ovule initiation and aggravated ovule abortion. There was no induction of carbon (C) starvation genes in the transgenic lines, and supplementing newly forming floral buds with extra C failed to recover the ovule phenotype. This indicates that suppression of CWIN did not lead to C starvation. A group of hexose transporters was downregulated in the transgenic plants. Among them, two representative ones were spatially coexpressed with CWIN2 and CWIN4, suggesting a coupling between CWIN and hexose transporters for ovule initiation. RNA-sequencing analysis identified differentially expressed genes encoding putative extracellular receptor-like kinases, MADS-box transcription factors, including STK, and early auxin response genes in response to CWIN-silencing. Our data demonstrate the essential role of CWIN in ovule initiation, which is most likely to occur through sugar signaling instead of C nutrient contribution. We propose that CWIN-mediated sugar signaling may be perceived by, and transmitted through, hexose transporters or receptor-like kinases to regulate ovule formation by modulating downstream auxin signaling and MADS-box transcription factors.

Highlights

In higher plants, most carbohydrate making up the bulk of the biomass and crop yield originates from sucrose (Suc), making Suc a crucial yield determinant (Ruan, 2014)
As the first step to address the potential involvement of cell wall invertase (CWIN) in ovule development, we performed in situ hybridization experiments to examine whether CWIN2 and CWIN4 were expressed in the cellular sites of ovule initiation
The analyses revealed that CWIN2 mRNA was detected in the inflorescence meristem and floral primordium (Figure 1A), in comparison with the sense control (Figure 1B)

Summary

Introduction

Most carbohydrate making up the bulk of the biomass and crop yield originates from sucrose (Suc), making Suc a crucial yield determinant (Ruan, 2014). Symplasmic transport through plasmodesmata (PD) is considered as a common pathway of Suc unloading, Suc can only be transported apoplasmically across cell wall matrix and plasma membranes in cellular interfaces lacking PD connection (Patrick, 1997). In this latter case, Suc is often unloaded from the sieve element-companion cell (SE/CC) to the surrounding cell wall matrix, and taken up by recipient sink cells via Suc transporters (SUT) or hexose transporters (HXT) following hydrolysis of Suc by CWIN at the extracellular space (Braun et al, 2014; Li et al, 2017)

Methods

Results

Conclusion