The transcription factors ZAT5 and BLH2/4 regulate homogalacturonan demethylesterification in Arabidopsis seed coat mucilage

Author:

Xie Minmin123ORCID,Ding Anming1ORCID,Guo Yongfeng1ORCID,Sun Jinhao14ORCID,Qiu Wanya15ORCID,Chen Mingli1ORCID,Li Zhiyuan1ORCID,Li Shanshan15ORCID,Zhou Gongke6ORCID,Xu Yan7ORCID,Wang Meng16ORCID,Richel Aurore3ORCID,Gong Daping1ORCID,Kong Yingzhen16ORCID

Affiliation:

1. Key Laboratory of Tobacco Gene Resources, Biotechnology Center, Tobacco Research Institute, Chinese Academy of Agricultural Sciences (CAAS) , Qingdao 266101 , China

2. Graduate School of Chinese Academy of Agricultural Science , Beijing 100081 , China

3. Laboratory of Biomass and Green Technologies, Gembloux Agro-Bio Tech, University of Liege , Gembloux 5030 , Belgium

4. Technology Center, China Tobacco Jiangsu Industrial Co., Ltd. , Nanjing 210019 , China

5. Key Laboratory of Natural Products Synthetic Biology of Ethnic Medicinal Endophytes, State Ethnic Affairs Commission, Yunnan Minzu University , Kunming 650031 , China

6. College of Agronomy, Qingdao Agricultural University , Qingdao 266109 , China

7. Key Laboratory of Biofuels, Qingdao Engineering Research Center of Biomass Resources and Environment, Qingdao Institute of Bioenergy and Bioprocess Technology, Chinese Academy of Sciences , Qingdao 266101 , China

Abstract

Abstract The level of methylesterification alters the functional properties of pectin, which is believed to influence plant growth and development. However, the mechanisms that regulate demethylesterification remain largely unexplored. Pectin with a high degree of methylesterification is produced in the Golgi apparatus and then transferred to the primary cell wall where it is partially demethylesterified by pectin methylesterases (PMEs). Here, we show that in Arabidopsis (Arabidopsis thaliana) seed mucilage, pectin demethylesterification is negatively regulated by the transcription factor ZINC FINGER FAMILY PROTEIN5 (ZAT5). Plants carrying null mutations in ZAT5 had increased PME activity, decreased pectin methylesterification, and produced seeds with a thinner mucilage layer. We provide evidence that ZAT5 binds to a TGATCA motif and thereby negatively regulates methylesterification by reducing the expression of PME5, HIGHLY METHYL ESTERIFIED SEEDS (HMS)/PME6, PME12, and PME16. We also demonstrate that ZAT5 physically interacts with BEL1-LIKE HOMEODOMAIN2 (BLH2) and BLH4 transcription factors. BLH2 and BLH4 are known to modulate pectin demethylesterification by directly regulating PME58 expression. The ZAT5–BLH2/4 interaction provides a mechanism to control the degree of pectin methylesterification in seed coat mucilage by modifying each transcription factor's ability to regulate the expression of target genes encoding PMEs. Taken together, these findings reveal a transcriptional regulatory module comprising ZAT5, BLH2, and BLH4, that functions in modulating the demethylesterification of homogalacturonan in seed coat mucilage.

Funder

National Natural Science Foundation of China

Key Science and Technology Project of the China National Tobacco Corporation

NSF

Publisher

Oxford University Press (OUP)

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