Genome-Wide Profiling and Phylogenetic Analysis of the SWEET Sugar Transporter Gene Family in Walnut and Their Lack of Responsiveness to Xanthomonas arboricola pv. juglandis Infection.

Shijiao Jiang,Shan Han,Sriema L Walawage,Aaron Jacobson,Bipin Balan,Charles A Leslie,Xueqin Wan,Cintia H D Sagawa,Abhaya M Dandekar,Renata De A B Assis,Le Wang,Lanlan Zhang,Steven H Lee,Paulo A Zaini,Leandro M Moreira

doi:10.3390/ijms21041251

Abstract

Following photosynthesis, sucrose is translocated to sink organs, where it provides the primary source of carbon and energy to sustain plant growth and development. Sugar transporters from the SWEET (sugar will eventually be exported transporter) family are rate-limiting factors that mediate sucrose transport across concentration gradients, sustain yields, and participate in reproductive development, plant senescence, stress responses, as well as support plant–pathogen interaction, the focus of this study. We identified 25 SWEET genes in the walnut genome and distinguished each by its individual gene structure and pattern of expression in different walnut tissues. Their chromosomal locations, cis-acting motifs within their 5′ regulatory elements, and phylogenetic relationship patterns provided the first comprehensive analysis of the SWEET gene family of sugar transporters in walnut. This family is divided into four clades, the analysis of which suggests duplication and expansion of the SWEET gene family in Juglans regia. In addition, tissue-specific gene expression signatures suggest diverse possible functions for JrSWEET genes. Although these are commonly used by pathogens to harness sugar products from their plant hosts, little was known about their role during Xanthomonas arboricola pv. juglandis (Xaj) infection. We monitored the expression profiles of the JrSWEET genes in different tissues of “Chandler” walnuts when challenged with pathogen Xaj417 and concluded that SWEET-mediated sugar translocation from the host is not a trigger for walnut blight disease development. This may be directly related to the absence of type III secretion system-dependent transcription activator-like effectors (TALEs) in Xaj417, which suggests different strategies are employed by this pathogen to promote susceptibility to this major aboveground disease of walnuts.

Highlights

Following photosynthesis, sugars like sucrose, transported from their photosynthetic “sources” to heterotrophic “sinks”, enable plant growth and development [1,2,3]
A proton-coupled sucrose transporter (SUT) that acts as a sugar/H+ symporter is essential for translocation [7], while a sieve element–companion cell complex (SE/CC) is required for translocation into the phloem
Since little is known about this plant–pathogen interaction, the current study examined the significance of SWEET genes as possible susceptibility genes, as occurs in rice bacterial leaf blight and other diseases caused by Xanthomonas

Summary

Introduction

Sugars like sucrose, transported from their photosynthetic “sources” to heterotrophic “sinks”, enable plant growth and development [1,2,3]. A proton-coupled sucrose transporter (SUT) that acts as a sugar/H+ symporter is essential for translocation [7], while a sieve element–companion cell complex (SE/CC) is required for translocation into the phloem. Another type of sugar transporter known as SWEETs (sugar will eventually be exported transporters) effuse sucrose from inside the cell into the cell wall as a prerequisite for SUT1-mediated phloem loading [1]. Since these sugar transporters regulate the sucrose pools in plants, several microorganisms vie for carbohydrates from plants through this pathway. Unlike SUTs, which are expressed at a low level, require energy, and are a rate-limiting factor for sucrose transport, SWEET proteins function as key transporters for sucrose, hexose, and fructose along a concentration gradient and become a priority target in plant–pathogen interactions [11,12,13]

Methods

Results

Conclusion