Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.

Terpenoids are critical components of plant environmental adaptation mechanisms. They also exhibit significant therapeutic potential in herbal medicine. 3-Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR), a pivotal rate-limiting enzyme governing the initial stage of the mevalonate (MVA) pathway...

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Main Authors: Xiaohan Tang, Xiaojun Ma, Jun Cao, Xinhong Wang, Xuexiang Li, Xiaozhou Yang, Jing Shu
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0330439
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author Xiaohan Tang
Xiaojun Ma
Jun Cao
Xinhong Wang
Xuexiang Li
Xiaozhou Yang
Jing Shu
author_facet Xiaohan Tang
Xiaojun Ma
Jun Cao
Xinhong Wang
Xuexiang Li
Xiaozhou Yang
Jing Shu
author_sort Xiaohan Tang
collection DOAJ
description Terpenoids are critical components of plant environmental adaptation mechanisms. They also exhibit significant therapeutic potential in herbal medicine. 3-Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR), a pivotal rate-limiting enzyme governing the initial stage of the mevalonate (MVA) pathway in triterpene saponin biosynthesis, remains uncharacterized in Ziziphus jujuba var. spinosa. Through genome-wide and molecular analysis, we systematically identified ZjHMGR isoforms and revealed differential tissue-specific expression patterns and significant salt stress-responsive regulation across identified isoforms. Our findings reveal three evolutionarily conserved ZjHMGR isoforms with a complete HMG-CoA reductase domain and closely related to Populus trichocarpa. Collinearity analysis revealed two collinear gene pairs, and purifying selection was identified as the primary evolutionary force acting on the ZjHMGR gene family. Cis-acting element analysis revealed that ZjHMGR gene family enriched MYB-related, TC-rich repeats, light- and hormone-responsive elements, suggesting transcriptional regulation by environmental stimuli and phytohormones. Spatiotemporal expression analysis via qRT-PCR revealed differential transcriptional patterns of ZjHMGR members, with pronounced upregulation under ABA, MeJA, and light induction. Saline stress disrupted the growth of wild jujube seedlings while activating ZjHMGR expression alongside other MVA pathway genes. Overexpression of ZjHMGR enhances salt stress resistance in Arabidopsis thaliana. This study lays the foundation for further investigations into the molecular mechanisms of the ZjHMGR gene family concerning saponin biosynthesis, phytohormone interactions, and salt tolerance in wild jujube.
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spelling doaj-art-cf43adc8d66f4d5b96c65213eb0c55782025-08-23T05:32:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01208e033043910.1371/journal.pone.0330439Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa. Xiaohan TangXiaojun MaJun CaoXinhong WangXuexiang LiXiaozhou YangJing ShuTerpenoids are critical components of plant environmental adaptation mechanisms. They also exhibit significant therapeutic potential in herbal medicine. 3-Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR), a pivotal rate-limiting enzyme governing the initial stage of the mevalonate (MVA) pathway in triterpene saponin biosynthesis, remains uncharacterized in Ziziphus jujuba var. spinosa. Through genome-wide and molecular analysis, we systematically identified ZjHMGR isoforms and revealed differential tissue-specific expression patterns and significant salt stress-responsive regulation across identified isoforms. Our findings reveal three evolutionarily conserved ZjHMGR isoforms with a complete HMG-CoA reductase domain and closely related to Populus trichocarpa. Collinearity analysis revealed two collinear gene pairs, and purifying selection was identified as the primary evolutionary force acting on the ZjHMGR gene family. Cis-acting element analysis revealed that ZjHMGR gene family enriched MYB-related, TC-rich repeats, light- and hormone-responsive elements, suggesting transcriptional regulation by environmental stimuli and phytohormones. Spatiotemporal expression analysis via qRT-PCR revealed differential transcriptional patterns of ZjHMGR members, with pronounced upregulation under ABA, MeJA, and light induction. Saline stress disrupted the growth of wild jujube seedlings while activating ZjHMGR expression alongside other MVA pathway genes. Overexpression of ZjHMGR enhances salt stress resistance in Arabidopsis thaliana. This study lays the foundation for further investigations into the molecular mechanisms of the ZjHMGR gene family concerning saponin biosynthesis, phytohormone interactions, and salt tolerance in wild jujube.https://doi.org/10.1371/journal.pone.0330439
spellingShingle Xiaohan Tang
Xiaojun Ma
Jun Cao
Xinhong Wang
Xuexiang Li
Xiaozhou Yang
Jing Shu
Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.
PLoS ONE
title Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.
title_full Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.
title_fullStr Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.
title_full_unstemmed Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.
title_short Genome-Wide identification and salt stress-responsive expression dynamics of the HMGR gene family in Ziziphus jujuba var. spinosa.
title_sort genome wide identification and salt stress responsive expression dynamics of the hmgr gene family in ziziphus jujuba var spinosa
url https://doi.org/10.1371/journal.pone.0330439
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