Stomatal density suppressor PagSDD1 is a "generalist" gene that promotes plant growth and improves water use efficiency

Yufei Xia; Qiang Han; Jianghai Shu; Shenxiu Jiang; Xiangyang Kang

doi:10.1016/j.ijbiomac.2024.129721

Stomatal density suppressor PagSDD1 is a "generalist" gene that promotes plant growth and improves water use efficiency

Int J Biol Macromol. 2024 Mar;262(Pt 1):129721. doi: 10.1016/j.ijbiomac.2024.129721. Epub 2024 Jan 29.

Authors

Yufei Xia¹, Qiang Han², Jianghai Shu³, Shenxiu Jiang⁴, Xiangyang Kang⁵

Affiliations

¹ State Key Laboratory of Tree Genetics and Breeding, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China. Electronic address: xiayufei@bjfu.edu.cn.
² Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, China. Electronic address: hanqiang1988@caf.ac.cn.
³ State Key Laboratory of Tree Genetics and Breeding, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China. Electronic address: shujianghai@bjfu.edu.cn.
⁴ State Key Laboratory of Tree Genetics and Breeding, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China. Electronic address: jiangsx@bjfu.edu.cn.
⁵ State Key Laboratory of Tree Genetics and Breeding, National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China. Electronic address: kangxy@bjfu.edu.cn.

PMID: 38296132
DOI: 10.1016/j.ijbiomac.2024.129721

Abstract

The serine protease SDD1 regulates stomatal density, but its potential impact on plant vegetative growth is unclear. Our study reveals a substantial upregulation of SDD1 in triploid poplar apical buds and leaves, suggesting its possible role in their growth regulation. We cloned PagSDD1 from poplar 84 K (Populus alba × P. glandulosa) and found that overexpression in poplar, soybean, and lettuce led to decreased leaf stomatal density. Furthermore, PagSDD1 represses PagEPF1, PagEPF2, PagEPFL9, PagSPCH, PagMUTE, and PagFAMA expression. In contrast, PagSDD1 promotes the expression of its receptors, PagTMM and PagERECTA. PagSDD1-OE poplars showed stronger drought tolerance than wild-type poplars. Simultaneously, PagSDD1-OE poplar, soybean, and lettuce had vegetative growth advantages. RNA sequencing revealed a significant upregulation of genes PagLHCB2.1 and PagGRF5, correlating positively with photosynthetic rate, and PagCYCA3;4 and PagEXPA8 linked to cell division and differentiation in PagSDD1-OE poplars. This increase promoted leaf photosynthesis, boosted auxin and cytokinin accumulation, and enhanced vegetative growth. SDD1 overexpression can increase the biomass of poplar, soybean, and lettuce by approximately 70, 176, and 155 %, respectively, and increase the water use efficiency of poplar leaves by over 52 %, which is of great value for the molecular design and breeding of plants with growth and water-saving target traits.

Keywords: Drought stress tolerance; PagSDD1; Poplar; Stomatal density; Vegetative growth; Water use efficiency.

MeSH terms

Droughts
Gene Expression Regulation, Plant
Plant Breeding
Plant Leaves / metabolism
Plant Stomata / genetics
Populus* / metabolism
Water* / metabolism

Substances

Water