Modification of Threonine-825 of SlBRI1 Enlarges Cell Size to Enhance Fruit Yield by Regulating the Cooperation of BR-GA Signaling in Tomato.

Shufen Wang,Dehai Liu,Shangtan Fu,Yu Pei,Miaomiao Hu,Siqi Lv,Meng Jiang,Shuhua Huang,Tong Zhao,Xiaofeng Wang

doi:10.3390/ijms22147673

Shufen Wang, Dehai Liu + Show 8 more

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https://doi.org/10.3390/ijms22147673

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Abstract

Brassinosteroids (BRs) are growth-promoting phytohormones that can efficiently function by exogenous application at micromolar concentrations or by endogenous fine-tuning of BR-related gene expression, thus, precisely controlling BR signal strength is a key factor in exploring the agricultural potential of BRs. BRASSINOSTEROID INSENSITIVE1 (BRI1), a BR receptor, is the rate-limiting enzyme in BR signal transduction, and the phosphorylation of each phosphorylation site of SlBRI1 has a distinct effect on BR signal strength and botanic characteristics. We recently demonstrated that modifying the phosphorylation sites of tomato SlBRI1 could improve the agronomic traits of tomato to different extents; however, the associated agronomic potential of SlBRI1 phosphorylation sites in tomato has not been fully exploited. In this research, the biological functions of the phosphorylation site threonine-825 (Thr-825) of SlBRI1 in tomato were investigated. Phenotypic analysis showed that, compared with a tomato line harboring SlBRI1, transgenic tomato lines expressing SlBRI1 with a nonphosphorylated Thr-825 (T825A) exhibited a larger plant size due to a larger cell size and higher yield, including a greater plant height, thicker stems, longer internodal lengths, greater plant expansion, a heavier fruit weight, and larger fruits. Molecular analyses further indicated that the autophosphorylation level of SlBRI1, BR signaling, and gibberellic acid (GA) signaling were elevated when SlBRI1 was dephosphorylated at Thr-825. Taken together, the results demonstrated that dephosphorylation of Thr-825 can enhance the functions of SlBRI1 in BR signaling, which subsequently activates and cooperates with GA signaling to stimulate cell elongation and then leads to larger plants and higher yields per plant. These results also highlight the agricultural potential of SlBRI1 phosphorylation sites for breeding high-yielding tomato varieties through precise control of BR signaling.

Highlights

Tomato (Solanum lycopersicum) is one of the most important vegetables worldwide, and fruit yield, including fruit number and fruit weight, is the major agronomic trait of concern for tomato breeding
Numerous studies have shown that whole tomato fruit growth is essentially based on cell division and expansion, which rely on multiple hormonal signals and relevant responsive genes [1,2,3]
SlBRI1 is a receptor kinase that exerts its biological function through phosphorylation, SlBRI1 is a receptor kinase that exerts its biological through phosphorylaand its phosphorylation sites have different effects onfunction the phosphorylation level and tion, and its phosphorylation sites have different effects on the phosphorylation level mediate the biological functions of SlBRI1 [29,30]

Summary

Introduction

Tomato (Solanum lycopersicum) is one of the most important vegetables worldwide, and fruit yield, including fruit number and fruit weight, is the major agronomic trait of concern for tomato breeding. The cell division stage is tightly controlled by cyclin-dependent kinases (CDKs) [4,5] Plant hormones such as auxin (indole3-acetic acid, IAA), gibberellic acids (GAs), and brassinosteroids (BRs) have been repeatedly demonstrated to be major regulators of cell division and expansion [6,7,8]. Exogenous application of these hormones and endogenous expression of their regulatory genes can alter both fruit growth and development in tomato [9,10,11]. In the presence of BRs, which are first perceived by BRI1, phosphorylation cascades of the signal components can activate the critical transcription factors

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