The GhSWEET42 Glucose Transporter Participates in Verticillium dahliae Infection in Cotton.

Mengxi Sun,Fei Zhang,Zhiqiang Zhang,Xiongfeng Ma,Daigang Yang,Hongjie Feng,Wenjie Sun,Xingxing Wang,Zhongying Ren,Wei Li,Junjie Zhao

doi:10.3389/fpls.2021.690754

Abstract

The SWEET (sugars will eventually be exported transporter) proteins, a family of sugar transporters, mediate sugar diffusion across cell membranes. Pathogenic fungi can acquire sugars from plant cells to satisfy their nutritional demands for growth and infection by exploiting plant SWEET sugar transporters. However, the mechanism underlying the sugar allocation in cotton plants infected by Verticillium dahliae, the causative agent of Verticillium wilt, remains unclear. In this study, observations of the colonization of cotton roots by V. dahliae revealed that a large number of conidia had germinated at 48-hour post-inoculation (hpi) and massive hyphae had appeared at 96 hpi. The glucose content in the infected roots was significantly increased at 48 hpi. On the basis of an evolutionary analysis, an association analysis, and qRT-PCR assays, GhSWEET42 was found to be closely associated with V. dahliae infection in cotton. Furthermore, GhSWEET42 was shown to encode a glucose transporter localized to the plasma membrane. The overexpression of GhSWEET42 in Arabidopsis thaliana plants led to increased glucose content, and compromised their resistance to V. dahliae. In contrast, knockdown of GhSWEET42 expression in cotton plants by virus-induced gene silencing (VIGS) led to a decrease in glucose content, and enhanced their resistance to V. dahliae. Together, these results suggest that GhSWEET42 plays a key role in V. dahliae infection in cotton through glucose translocation, and that manipulation of GhSWEET42 expression to control the glucose level at the infected site is a useful method for inhibiting V. dahliae infection.

Highlights

Verticillium dahliae is a soil-borne fungal pathogen that can infect a broad range of plant species, including many economically important crops, and causes devastating diseases (Fradin and Thomma, 2006)
From 0 to 12 hpi, no obvious green fluorescence was detected in the cotton roots, implying that V. dahliae did not infect the roots before 12 hpi (Figures 1A–C and Supplementary Figure 1)
V. dahliae needs to penetrate the root epidermal cells to complete the colonization process, and this stage is critical for successful infection by V. dahliae (Bowers et al, 1996)

Summary

Introduction

Verticillium dahliae is a soil-borne fungal pathogen that can infect a broad range of plant species, including many economically important crops, and causes devastating diseases (Fradin and Thomma, 2006). V. dahliae hyphae pass through the epidermal cells and multiply in the vascular tissue (Zhao et al, 2014). The hyphae produce toxins and block plant ducts, thereby disrupting water transport, and leading to plant death (Fradin and Thomma, 2006). GhSWEET42 Participates in Fungal Infection to meet the nutrient requirements for growth (Yamada et al, 2016). Since carbon is essential for growth and pathogenicity, obtaining sufficient sugars from plants is an important task for successful infection by plant pathogens (Chen et al, 2010; Klimes et al, 2015). Little is known about the molecular mechanism of sugar uptake by V. dahliae from plants

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