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, Qing Ma State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Hai-Shuang Liu State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Hu-Jun Li State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Wan-Peng Bai State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Qi-Fei Gao School of Agriculture and Biology, Shanghai Jiao Tong University , Shanghai 200240 , China Department of Plant and Microbial Biology, University of California , Berkeley, CA 94720 , USA Search for other works by this author on: Oxford Academic Sheng-Dan Wu State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Ecology, Lanzhou University , Lanzhou 730000 , China Search for other works by this author on: Oxford Academic Xiu-Xia Yin State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Qin-Qin Chen State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Ya-Qi Shi State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Tian-Ge Gao State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic
https://orcid.org/0000-0002-7777-6830 , Ai-Ke Bao State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Hong-Ju Yin State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Search for other works by this author on: Oxford Academic Li Li Institute of Grassland, Xinjiang Academy of Animal Science , Urumqi 830000 , China Search for other works by this author on: Oxford Academic Owen Rowland Department of Biology and Institute of Biochemistry, Carleton University , Ottawa, Ontario K1S 5B6 , Search for other works by this author on: Oxford Academic Shelley R Hepworth Department of Biology and Institute of Biochemistry, Carleton University , Ottawa, Ontario K1S 5B6 , Canada Search for other works by this author on: Oxford Academic Sheng Luan Department of Plant and Microbial Biology, University of California , Berkeley, CA 94720 , USA Search for other works by this author on: Oxford Academic Suo-Min Wang State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems; College of Pastoral Agriculture Science and Technology, Lanzhou University , Lanzhou 730020 , China Author for correspondence: smwang@lzu.edu.cn (S.M.W.) Search for other works by this author on: Oxford Academic
Plant Physiology, Volume 195, Issue 1, May 2024, Pages 617–639, https://doi.org/10.1093/plphys/kiae040
Published:
29 January 2024
Article history
Received:
26 September 2023
Accepted:
21 December 2023
Published:
29 January 2024
Corrected and typeset:
19 February 2024
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Qing Ma, Hai-Shuang Liu, Hu-Jun Li, Wan-Peng Bai, Qi-Fei Gao, Sheng-Dan Wu, Xiu-Xia Yin, Qin-Qin Chen, Ya-Qi Shi, Tian-Ge Gao, Ai-Ke Bao, Hong-Ju Yin, Li Li, Owen Rowland, Shelley R Hepworth, Sheng Luan, Suo-Min Wang, Genomic analysis reveals phylogeny of Zygophyllales and mechanism for water retention of a succulent xerophyte, Plant Physiology, Volume 195, Issue 1, May 2024, Pages 617–639, https://doi.org/10.1093/plphys/kiae040
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Abstract
Revealing the genetic basis for stress-resistant traits in extremophile plants will yield important information for crop improvement. Zygophyllum xanthoxylum, an extant species of the ancient Mediterranean, is a succulent xerophyte that can maintain a favorable water status under desert habitats; however, the genetic basis of this adaptive trait is poorly understood. Furthermore, the phylogenetic position of Zygophyllales, to which Z. xanthoxylum belongs, remains controversial. In this study, we sequenced and assembled the chromosome-level genome of Z. xanthoxylum. Phylogenetic analysis showed that Zygophyllales and Myrtales form a separated taxon as a sister to the clade comprising fabids and malvids, clarifying the phylogenetic position of Zygophyllales at whole-genome scale. Analysis of genomic and transcriptomic data revealed multiple critical mechanisms underlying the efficient osmotic adjustment using Na+ and K+ as “cheap" osmolytes that Z. xanthoxylum has evolved through the expansion and synchronized expression of genes encoding key transporters/channels and their regulators involved in Na+/K+ uptake, transport, and compartmentation. It is worth noting that ZxCNGC1;1 (cyclic nucleotide-gated channels) and ZxCNGC1;2 constituted a previously undiscovered energy-saving pathway for Na+ uptake. Meanwhile, the core genes involved in biosynthesis of cuticular wax also featured an expansion and upregulated expression, contributing to the water retention capacity of Z. xanthoxylum under desert environments. Overall, these findings boost the understanding of evolutionary relationships of eudicots, illustrate the unique water retention mechanism in the succulent xerophyte that is distinct from glycophyte, and thus provide valuable genetic resources for the improvement of stress tolerance in crops and insights into the remediation of sodic lands.
© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/pages/standard-publication-reuse-rights)
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