The miR396a–SlGRF8 module regulates sugar accumulation in the roots via SlSTP10 during the interaction between root-knot nematodes and tomato plants

doi:10.1111/jipb.13794

J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (12): 2701-2715.DOI: 10.1111/jipb.13794 cstr: 32098.14.jipb.13794

• Molecular Physiology • Previous Articles Next Articles

The miR396a–SlGRF8 module regulates sugar accumulation in the roots via SlSTP10 during the interaction between root-knot nematodes and tomato plants

Lulu Sun^1,2†, Mengting Zhu^1,2†, Xiaoxuan Zhou^1,2†, Ruiyue Gu^1,2, Yuying Hou^1,2, Tongtong Li^1,2, Huang Huang^1,2, Rui Yang^1,2, Shaohui Wang^1,2* and Wenchao Zhao^1,2*

1. College of Plant Science and Technology, Beijing University of Agriculture, Beijing 102206, China
2. Beijing Key Laboratory for Agricultural Application and New Technique, Beijing University of Agriculture, Beijing 102206, China
^†These authors contributed equally to this work.
^*Correspondences: Shaohui Wang (wangshaohui@bua.edu.cn); Wenchao Zhao (zwcxy1985@163.com, Dr. Zhao is fully responsible for the distribution of all materials associated with this article in the manuscript)

Received:2024-01-15 Accepted:2024-09-26 Online:2024-10-25 Published:2024-12-01
Supported by:
This work was supported by the Beijing Natural Science Foundation (6222005, 6242006), the National Natural Science Foundation of China (32002117, 32372796), the R&D Program of Beijing Municipal Education Commission (KZ20231002033), the Beijing Municipal University classified development project (11000024T000002961733), the Beijing Innovation Consortium of Agriculture Research System (BAIC01‐2024), the Science and Technology Innovation Support Program of Beijing University of Agriculture (BUA‐HHXD2023).

Abstract

Abstract: Root-knot nematodes (RKNs; Meloidogyne spp.) are a serious threat to crop production. The competition between plants and pathogens for assimilates influences the outcome of their interactions. However, the mechanisms by which plants and nematodes compete with each other for assimilates have not been elucidated. In this study, we demonstrated that miR396a plays a negative role in defense against RKNs and a positive role in sugar accumulation in tomato roots. The overexpression of SlGRF8 (Solanum lycopersicum growth-regulating factor 8), the target of miR396a, decreased the sugar content of the roots and the susceptibility to RKNs, whereas the grf8-cr mutation had the opposite effects. Furthermore, we confirmed that SlGRF8 regulated the sugar content in roots by directly activating the transcription of SlSTP10 (Solanum lycopersicum sugar transporter protein 10) in response to RKN stress. Moreover, SlSTP10 was expressed primarily in the tissues surrounding giant cells, and the SlSTP10 knockout increased both the sugar content in the roots and the plant's susceptibility to RKNs. Overall, this study provides important insight into the molecular mechanism through which the miR396a-SlGRF8-SlSTP10 module regulates sugar allocation in roots under RKN stress.

Key words: miR396a, SlGRF8, SlSTP10, tomato, root‐knot nem-atode, sugar

Lulu Sun, Mengting Zhu, Xiaoxuan Zhou, Ruiyue Gu, Yuying Hou, Tongtong Li, Huang Huang, Rui Yang, Shaohui Wang, Wenchao Zhao. The miR396a–SlGRF8 module regulates sugar accumulation in the roots via SlSTP10 during the interaction between root-knot nematodes and tomato plants[J]. J Integr Plant Biol., 2024, 66(12): 2701-2715.

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The miR396a–SlGRF8 module regulates sugar accumulation in the roots via SlSTP10 during the interaction between root-knot nematodes and tomato plants

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