HO Drives the Transition from Conchocelis to Conchosporangia in the Red Alga with Promotion Facilitated by 1-Aminocyclopropane-1-carboxylic Acid

Overview

Journal Front Plant Sci

Date 2024 Mar 27

PMID 38533401

Authors

Tingting Niu

Haike Qian

Haimin Chen

Qijun Luo

Juanjuan Chen

Rui Yang

Peng Zhang

Tiegan Wang

Affiliations

Soon will be listed here.

Abstract

The Bangiales represent an ancient lineage within red algae that are characterized by a life history featuring a special transitional stage from diploid to haploid known as the conchosporangia stage. However, the regulatory mechanisms governing the initiation of this stage by changes in environmental conditions are not well understood. This study analyzed the changes in phytohormones and HO content during the development of conchosporangia. It also compared the gene expression changes in the early development of conchosporangia through transcriptome analysis. The findings revealed that HO was shown to be the key signal initiating the transition from conchocelis to conchosporangia in . Phytohormone analysis showed a significant increase in 1-aminocylopropane-1-carboxylic acid (ACC) levels during conchosporangia maturation, while changes in environmental conditions were found to promote the rapid release of HO. HO induction led to conchosporangia development, and ACC enhanced both HO production and conchosporangia development. This promotive effect was inhibited by the NADPH oxidase inhibitor diphenylene iodonium and the HO scavenger N, N'-dimethylthiourea. The balance of oxidative-antioxidative mechanisms was maintained by regulating the activities and transcriptional levels of enzymes involved in HO production and scavenging. Transcriptome analysis in conjunction with evaluation of enzyme and transcription level changes revealed upregulation of protein and sugar synthesis along with modulation of energy supply under the conditions that induced maturation, and exogenous ACC was found to enhance the entire process. Overall, this study demonstrates that ACC enhances HO promotion of the life cycle switch responsible for the transition from a vegetative conchocelis to a meiosis-preceding conchosporangia stage in Bangiales species.

References

Garcia-Jimenez P, Montero-Fernandez M, Robaina R . Molecular mechanisms underlying Grateloupia imbricata (Rhodophyta) carposporogenesis induced by methyl jasmonate. J Phycol. 2017; 53(6):1340-1344. DOI: 10.1111/jpy.12594. View

Van de Poel B, Van Der Straeten D . 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene!. Front Plant Sci. 2014; 5:640. PMC: 4227472. DOI: 10.3389/fpls.2014.00640. View

Pertea M, Pertea G, Antonescu C, Chang T, Mendell J, Salzberg S . StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015; 33(3):290-5. PMC: 4643835. DOI: 10.1038/nbt.3122. View

Xin P, Guo Q, Li B, Cheng S, Yan J, Chu J . A Tailored High-Efficiency Sample Pretreatment Method for Simultaneous Quantification of 10 Classes of Known Endogenous Phytohormones. Plant Commun. 2020; 1(3):100047. PMC: 7747986. DOI: 10.1016/j.xplc.2020.100047. View

Weyers J, Paterson N . Plant hormones and the control of physiological processes. New Phytol. 2021; 152(3):375-407. DOI: 10.1046/j.0028-646X.2001.00281.x. View

Mikami K, Takahashi M . Life cycle and reproduction dynamics of Bangiales in response to environmental stresses. Semin Cell Dev Biol. 2022; 134:14-26. DOI: 10.1016/j.semcdb.2022.04.004. View

Borg M, Krueger-Hadfield S, Destombe C, Collen J, Lipinska A, Coelho S . Red macroalgae in the genomic era. New Phytol. 2023; 240(2):471-488. DOI: 10.1111/nph.19211. View

Garcia-Jimenez P, Robaina R . EFFECTS OF ETHYLENE ON TETRASPOROGENESIS IN PTEROCLADIELLA CAPILLACEA (RHODOPHYTA)(1). J Phycol. 2016; 48(3):710-5. DOI: 10.1111/j.1529-8817.2012.01156.x. View

Takahashi M, Mikami K . Oxidative Stress Promotes Asexual Reproduction and Apogamy in the Red Seaweed . Front Plant Sci. 2017; 8:62. PMC: 5270553. DOI: 10.3389/fpls.2017.00062. View

10.

Vanderstraeten L, Van Der Straeten D . Accumulation and Transport of 1-Aminocyclopropane-1-Carboxylic Acid (ACC) in Plants: Current Status, Considerations for Future Research and Agronomic Applications. Front Plant Sci. 2017; 8:38. PMC: 5258695. DOI: 10.3389/fpls.2017.00038. View

11.

Li Y, Qi M, Zhang Q, Xu Z, Zhang Y, Gao Y . Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants. J Fungi (Basel). 2023; 9(1). PMC: 9866368. DOI: 10.3390/jof9010055. View

12.

Taya K, Takeuchi S, Takahashi M, Hayashi K, Mikami K . Auxin Regulates Apical Stem Cell Regeneration and Tip Growth in the Marine Red Alga . Cells. 2022; 11(17). PMC: 9454478. DOI: 10.3390/cells11172652. View

13.

Martinez-Garcia M, van der Maarel M . Floridoside production by the red microalga Galdieria sulphuraria under different conditions of growth and osmotic stress. AMB Express. 2016; 6(1):71. PMC: 5020028. DOI: 10.1186/s13568-016-0244-6. View

14.

Xia X, Zhou Y, Shi K, Zhou J, Foyer C, Yu J . Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot. 2015; 66(10):2839-56. DOI: 10.1093/jxb/erv089. View

15.

Lin Y, Xu K, Xu Y, Ji D, Chen C, Wang W . Transcriptome Co-expression Network Analysis Identifies Key Genes Regulating Conchosporangia Maturation of . Front Genet. 2021; 12:680120. PMC: 8278576. DOI: 10.3389/fgene.2021.680120. View

16.

Tsuchisaka A, Yu G, Jin H, Alonso J, Ecker J, Zhang X . A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics. 2009; 183(3):979-1003. PMC: 2778992. DOI: 10.1534/genetics.109.107102. View

17.

Garcia-Jimenez P, Montero-Fernandez M, Robaina R . Analysis of ethylene-induced gene regulation during carposporogenesis in the red seaweed Grateloupia imbricata (Rhodophyta). J Phycol. 2018; 54(5):681-689. DOI: 10.1111/jpy.12762. View

18.

Guzman-Uriostegui A, Robaina R, Freile-Pelegrin Y, Robledo D . Polyamines increase carpospore output and growth during in vitro cultivation of Hydropuntia cornea. Biotechnol Lett. 2011; 34(4):755-61. DOI: 10.1007/s10529-011-0823-1. View

19.

Mikami K, Li C, Irie R, Hama Y . A unique life cycle transition in the red seaweed depends on apospory. Commun Biol. 2019; 2:299. PMC: 6685973. DOI: 10.1038/s42003-019-0549-5. View

20.

Uji T, Endo H, Mizuta H . Sexual Reproduction a 1-Aminocyclopropane-1-Carboxylic Acid-Dependent Pathway Through Redox Modulation in the Marine Red Alga (Rhodophyta). Front Plant Sci. 2020; 11:60. PMC: 7028691. DOI: 10.3389/fpls.2020.00060. View