Liverwort bHLH transcription factors and the origin of stomata in plants

Guanxiao Chang; Jianchao Ma; Shuanghua Wang; Mengmeng Tang; Bo Zhang; Yadi Ma; Lijuan Li; Guiling Sun; Shanshan Dong; Yang Liu; Yun Zhou; Xiangyang Hu; Chun-Peng Song; Jinling Huang

doi:10.1016/j.cub.2023.05.050

Liverwort bHLH transcription factors and the origin of stomata in plants

Curr Biol. 2023 Jul 10;33(13):2806-2813.e6. doi: 10.1016/j.cub.2023.05.050. Epub 2023 Jun 14.

Authors

Guanxiao Chang¹, Jianchao Ma¹, Shuanghua Wang², Mengmeng Tang¹, Bo Zhang¹, Yadi Ma¹, Lijuan Li¹, Guiling Sun¹, Shanshan Dong³, Yang Liu⁴, Yun Zhou¹, Xiangyang Hu⁵, Chun-Peng Song⁶, Jinling Huang⁷

Affiliations

¹ State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China.
² Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China.
³ Fairy Lake Botanical Garden, Chinese Academy of Sciences, Shenzhen 518004, China.
⁴ Fairy Lake Botanical Garden, Chinese Academy of Sciences, Shenzhen 518004, China; BGI-Shenzhen, Shenzhen 518083, China.
⁵ College of Life Sciences, Shanghai University, Shanghai 200444, China.
⁶ State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China. Electronic address: songcp@henu.edu.cn.
⁷ State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China; Department of Biology, East Carolina University, Greenville, NC 27858, USA. Electronic address: huangj@ecu.edu.

PMID: 37321212
DOI: 10.1016/j.cub.2023.05.050

Abstract

Stomata are distributed in nearly all major groups of land plants, with the only exception being liverworts. Instead of having stomata on sporophytes, many complex thalloid liverworts possess air pores in their gametophytes. At present, whether stomata in land plants are derived from a common origin remains under debate.¹^,²^,³ In Arabidopsis thaliana, a core regulatory module for stomatal development comprises members of the bHLH transcription factor (TF) family, including AtSPCH, AtMUTE, and AtFAMA of subfamily Ia and AtSCRM1/2 of subfamily IIIb. Specifically, AtSPCH, AtMUTE, and AtFAMA each successively form heterodimers with AtSCRM1/2, which in turn regulate the entry, division, and differentiation of stomatal lineages.⁴^,⁵^,⁶^,⁷ In the moss Physcomitrium patens, two SMF (SPCH, MUTE and FAMA) orthologs have been characterized, one of which is functionally conserved in regulating stomatal development.⁸^,⁹ We here provide experimental evidence that orthologous bHLH TFs in the liverwort Marchantia polymorpha affect air pore spacing as well as the development of the epidermis and gametangiophores. We found that the bHLH Ia and IIIb heterodimeric module is highly conserved in plants. Genetic complementation experiments showed that liverwort SCRM and SMF genes weakly restored a stomata phenotype in atscrm1, atmute, and atfama mutant backgrounds in A. thaliana. In addition, homologs of stomatal development regulators FLP and MYB88 also exist in liverworts and weakly rescued the stomatal phenotype of atflp/myb88 double mutant. These results provide evidence not only for a common origin of all stomata in extant plants but also for relatively simple stomata in the ancestral plant.

Keywords: air chambers; air pores; evo-devo; gametangiophores; plant evolution; stomatal evolution.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Arabidopsis Proteins* / genetics
Arabidopsis Proteins* / metabolism
Arabidopsis*
Basic Helix-Loop-Helix Transcription Factors / genetics
Basic Helix-Loop-Helix Transcription Factors / metabolism
Gene Expression Regulation, Plant
Hepatophyta* / genetics
Hepatophyta* / metabolism
Plant Stomata / physiology
Plants / metabolism

Substances

Basic Helix-Loop-Helix Transcription Factors
Arabidopsis Proteins