AtSWEET1 negatively regulates plant susceptibility to root-knot nematode disease

Yuan Zhou; Dan Zhao; Yuxi Duan; Lijie Chen; Haiyan Fan; Yuanyuan Wang; Xiaoyu Liu; Li-Qing Chen; Yuanhu Xuan; Xiaofeng Zhu

doi:10.3389/fpls.2023.1010348

AtSWEET1 negatively regulates plant susceptibility to root-knot nematode disease

Front Plant Sci. 2023 Feb 7:14:1010348. doi: 10.3389/fpls.2023.1010348. eCollection 2023.

Authors

Yuan Zhou¹, Dan Zhao², Yuxi Duan¹, Lijie Chen¹, Haiyan Fan¹, Yuanyuan Wang³, Xiaoyu Liu⁴, Li-Qing Chen⁵, Yuanhu Xuan¹, Xiaofeng Zhu¹

Affiliations

¹ Nematology Institute of Northern China, College of Plant Protection, Shenyang Agriculture University, Shenyang, China.
² College of Plant Protection, Jilin Agricultural University, Changchun, China.
³ College of Biological Science and Technology, Shenyang Agriculture University, Shenyang, China.
⁴ College of Sciences, Shenyang Agriculture University, Shenyang, China.
⁵ Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, United States.

Abstract

The root-knot nematode Meloidogyne incognita is a pathogenic pest that causes severe economic loss to agricultural production by forming a parasitic relationship with its hosts. During the development of M. incognita in the host plant roots, giant cells are formed as a nutrient sink. However, the roles of sugar transporters during the giant cells gain sugar from the plant cells are needed to improve. Meanwhile, the eventual function of sugars will eventually be exported transporters (SWEETs) in nematode-plant interactions remains unclear. In this study, the expression patterns of Arabidopsis thaliana SWEETs were examined by inoculation with M. incognita at 3 days post inoculation (dpi) (penetration stage) and 18 dpi (developing stage). We found that few AtSWEETs responded sensitively to M. incognita inoculation, with the highest induction of AtSWEET1 (AT1G21460), a glucose transporter gene. Histological analyses indicated that the β-glucuronidase (GUS) and green fluorescent protein (GFP) signals were observed specifically in the galls of AtSWEET1-GUS and AtSWEET1-GFP transgenic plant roots, suggesting that AtSWEET1 was induced specifically in the galls. Genetic studies have shown that parasitism of M. incognita was significantly affected in atsweet1 compared to wild-type and complementation plants. In addition, parasitism of M. incognita was significantly affected in atsweet10 but not in atsweet13 and atsweet14, expression of which was induced by inoculation with M. incognita. Taken together, these data prove that SWEETs play important roles in plant and nematode interactions.

Keywords: Arabidopsis thaliana; Meloidogyne incognita; gene expression; giant cells; sugar transporters.

Grants and funding

This research was funded by the National Natural Science Foundation of China (32272499), the National Parasitic Resources Center (abbreviation number: NPRC-2019-194-30), and supported by the China Agriculture Research System of MOF and MARA(CARS-04-PS13) and the Research Foundation of Education Bureau of Liaoning Province, China (LJKZ0644).