Coevolution of Tandemly Repeated and RpaB-like Transcriptional Factor Confers Desiccation Tolerance to Subaerial Species

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2022 Oct 10

PMID 36215485

Authors

Hai-Feng Xu

Guo-Zheng Dai

Yang Bai

Jin-Long Shang

Bin Zheng

De-Min Ye

Huazhong Shi

Aaron Kaplan

Bao-Sheng Qiu

Affiliations

Soon will be listed here.

Abstract

Desert-inhabiting cyanobacteria can tolerate extreme desiccation and quickly revive after rehydration. The regulatory mechanisms that enable their vegetative cells to resurrect upon rehydration are poorly understood. In this study, we identified a single gene family of high light-inducible proteins (Hlips) with dramatic expansion in the genome and found an intriguingly special convergence formed through four tandem gene duplication. The emerged four independent genes form a gene cluster () and respond to dehydration positively. The gene mutants in were successfully generated by using gene-editing technology. Phenotypic analysis showed that the desiccation tolerance of -deleted mutant decreased significantly due to impaired photosystem II repair, whereas heterologous expression of from enhanced desiccation tolerance in sp. PCC 7120. Furthermore, a transcription factor Hrf1 ( repressor factor 1) was identified and shown to coordinately regulate the expression of and desiccation-induced . Hrf1 acts as a negative regulator for the adaptation of to the harsh desert environment. Phylogenetic analysis revealed that most species in the genus possess both tandemly repeated Hlips and Hrf1. Our results suggest convergent evolution of desiccation tolerance through the coevolution of tandem Hlips duplication and Hrf1 in subaerial species, providing insights into the mechanism of desiccation tolerance in photosynthetic organisms.

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References

Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A . Light-induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One. 2010; 5(6):e11000. PMC: 2882322. DOI: 10.1371/journal.pone.0011000. View

Lopez-Redondo M, Moronta F, Salinas P, Espinosa J, Cantos R, Dixon R . Environmental control of phosphorylation pathways in a branched two-component system. Mol Microbiol. 2010; 78(2):475-89. DOI: 10.1111/j.1365-2958.2010.07348.x. View

Oliver M, Jain R, Balbuena T, Agrawal G, Gasulla F, Thelen J . Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochemistry. 2010; 72(10):1273-84. DOI: 10.1016/j.phytochem.2010.10.020. View

Boothby T, Tapia H, Brozena A, Piszkiewicz S, Smith A, Giovannini I . Tardigrades Use Intrinsically Disordered Proteins to Survive Desiccation. Mol Cell. 2017; 65(6):975-984.e5. PMC: 5987194. DOI: 10.1016/j.molcel.2017.02.018. View

Xu H, Dai G, Qiu B . Weak red light plays an important role in awakening the photosynthetic machinery following desiccation in the subaerial cyanobacterium Nostoc flagelliforme. Environ Microbiol. 2019; 21(7):2261-2272. DOI: 10.1111/1462-2920.14600. View

Xiao L, Yang G, Zhang L, Yang X, Zhao S, Ji Z . The resurrection genome of Boea hygrometrica: A blueprint for survival of dehydration. Proc Natl Acad Sci U S A. 2015; 112(18):5833-7. PMC: 4426394. DOI: 10.1073/pnas.1505811112. View

Feng Y, Zhang Z, Feng J, Qiu B . Effects of UV-B radiation and periodic desiccation on the morphogenesis of the edible terrestrial cyanobacterium Nostoc flagelliforme. Appl Environ Microbiol. 2012; 78(19):7075-81. PMC: 3457489. DOI: 10.1128/AEM.01427-12. View

Oliver M, Farrant J, Hilhorst H, Mundree S, Williams B, Bewley J . Desiccation Tolerance: Avoiding Cellular Damage During Drying and Rehydration. Annu Rev Plant Biol. 2020; 71:435-460. DOI: 10.1146/annurev-arplant-071219-105542. View

Xu H, Dai G, Wang Y, Cheng C, Shang J, Li R . Expansion of bilin-based red light sensors in the subaerial desert cyanobacterium Nostoc flagelliforme. Environ Microbiol. 2022; 24(4):2047-2058. DOI: 10.1111/1462-2920.15932. View

10.

Rajeev L, da Rocha U, Klitgord N, Luning E, Fortney J, Axen S . Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISME J. 2013; 7(11):2178-91. PMC: 3806265. DOI: 10.1038/ismej.2013.83. View

11.

Wang Q, Jantaro S, Lu B, Majeed W, Bailey M, He Q . The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol. 2008; 147(3):1239-50. PMC: 2442545. DOI: 10.1104/pp.108.121087. View

12.

VanBuren R, Wai C, Pardo J, Giarola V, Ambrosini S, Song X . Desiccation Tolerance Evolved through Gene Duplication and Network Rewiring in . Plant Cell. 2018; 30(12):2943-2958. PMC: 6354263. DOI: 10.1105/tpc.18.00517. View

13.

Chavez Montes R, Haber A, Pardo J, Powell R, Divisetty U, Silva A . A comparative genomics examination of desiccation tolerance and sensitivity in two sister grass species. Proc Natl Acad Sci U S A. 2022; 119(5). PMC: 8812550. DOI: 10.1073/pnas.2118886119. View

14.

Oren N, Raanan H, Murik O, Keren N, Kaplan A . Dawn illumination prepares desert cyanobacteria for dehydration. Curr Biol. 2017; 27(19):R1056-R1057. DOI: 10.1016/j.cub.2017.08.027. View

15.

He Q, Dolganov N, Bjorkman O, Grossman A . The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem. 2000; 276(1):306-14. DOI: 10.1074/jbc.M008686200. View

16.

Wolk C, Vonshak A, Kehoe P, Elhai J . Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria. Proc Natl Acad Sci U S A. 1984; 81(5):1561-5. PMC: 344877. DOI: 10.1073/pnas.81.5.1561. View

17.

Bar Eyal L, Choubeh R, Cohen E, Eisenberg I, Tamburu C, Dorogi M . Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria. Proc Natl Acad Sci U S A. 2017; 114(35):9481-9486. PMC: 5584450. DOI: 10.1073/pnas.1708206114. View

18.

Chen M, Teng W, Zhao L, Hu C, Zhou Y, Han B . Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation. ISME J. 2020; 15(1):211-227. PMC: 7852516. DOI: 10.1038/s41396-020-00775-z. View

19.

Wang P, Grimm B . Connecting Chlorophyll Metabolism with Accumulation of the Photosynthetic Apparatus. Trends Plant Sci. 2021; 26(5):484-495. DOI: 10.1016/j.tplants.2020.12.005. View

20.

VanBuren R, Pardo J, Wai C, Evans S, Bartels D . Massive Tandem Proliferation of ELIPs Supports Convergent Evolution of Desiccation Tolerance across Land Plants. Plant Physiol. 2019; 179(3):1040-1049. PMC: 6393792. DOI: 10.1104/pp.18.01420. View