H2O2 drives the transition from conchocelis to conchosporangia in the red alga Pyropia haitanensis with promotion facilitated by 1-Aminocyclopropane-1-carboxylic acid

Tingting Niu; Haike Qian; Haimin Chen; Qijun Luo; Juanjuan Chen; Rui Yang; Peng Zhang; Tiegan Wang

doi:10.3389/fpls.2024.1379428

H₂O₂ drives the transition from conchocelis to conchosporangia in the red alga Pyropia haitanensis with promotion facilitated by 1-Aminocyclopropane-1-carboxylic acid

Front Plant Sci. 2024 Mar 12:15:1379428. doi: 10.3389/fpls.2024.1379428. eCollection 2024.

Authors

Tingting Niu^#¹, Haike Qian^#¹, Haimin Chen^{1

2}, Qijun Luo¹, Juanjuan Chen^{1

2}, Rui Yang^{1

2}, Peng Zhang³, Tiegan Wang³

Affiliations

¹ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, Zhejiang, China.
² Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, Ningbo University, Ningbo, Zhejiang, China.
³ Department of Genetic breeding, Zhejiang Mariculture Research Institute, Wenzhou, China.

^# Contributed equally.

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 H₂O₂ 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 H₂O₂ was shown to be the key signal initiating the transition from conchocelis to conchosporangia in Pyropia haitanensis. 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 H₂O₂. H₂O₂ induction led to conchosporangia development, and ACC enhanced both H₂O₂ production and conchosporangia development. This promotive effect was inhibited by the NADPH oxidase inhibitor diphenylene iodonium and the H₂O₂ scavenger N, N'-dimethylthiourea. The balance of oxidative-antioxidative mechanisms was maintained by regulating the activities and transcriptional levels of enzymes involved in H₂O₂ 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 H₂O₂ promotion of the life cycle switch responsible for the transition from a vegetative conchocelis to a meiosis-preceding conchosporangia stage in Bangiales species.

Keywords: 1-Aminocyclopropane-1-carboxylic acid; H2O2; Pyropia haitanensis; conchosporangia; life cycle.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This project was funded by NSFC (32373099), Key Scientific and Technological Grant of Zhejiang for Breeding New Agricultural (Aquaculture) Varieties (2021C02069-9), Major Scientific and Technological Project of Ningbo (2021Z004, 2021Z103), China Agriculture Research System of MOF and MARA.