Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone

The microfilament (MF) cytoskeleton, present in all eukaryotic cells, is not only essential for fundamental cellular processes but also is important in sensing and transducing external signals in response to various developmental cues and abiotic stresses. Neopyropia yezoensis, a species of seaweed...

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Main Authors: Jiqiang Yin, Ying Sun, Xinping Miao, Jiaxin Qu, Kunjie Zhang, Xue qing Han, Yichi Li, Jiahui Sun, Fanna Kong
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Plant Stress
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Online Access:http://www.sciencedirect.com/science/article/pii/S2667064X25000272
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author Jiqiang Yin
Ying Sun
Xinping Miao
Jiaxin Qu
Kunjie Zhang
Xue qing Han
Yichi Li
Jiahui Sun
Fanna Kong
author_facet Jiqiang Yin
Ying Sun
Xinping Miao
Jiaxin Qu
Kunjie Zhang
Xue qing Han
Yichi Li
Jiahui Sun
Fanna Kong
author_sort Jiqiang Yin
collection DOAJ
description The microfilament (MF) cytoskeleton, present in all eukaryotic cells, is not only essential for fundamental cellular processes but also is important in sensing and transducing external signals in response to various developmental cues and abiotic stresses. Neopyropia yezoensis, a species of seaweed belonging to the Rhodophyta, is an important macroalga that thrives in the intertidal zone. However, it remains uncertain whether the MF cytoskeleton of seaweed contributes to adaption to desiccation and rehydration. In this study, we present for the first time the evidence regarding the role of MFs in the desiccation tolerance of N. yezoensis. The organization and arrangement of MFs were significantly influenced by variations in the water content within thallus cells. Desiccation of the thallus induced changes of many actin and actin binding proteins (ABPs) at transcriptional, translational and post-translational phosphorylation levels. Notably, nine phosphosites from four proteins (actin, formin, septin, and fascin) showed changes in phosphorylation conditions. This indicate that phosphorylation modification was involved in MFs response to desiccation and rehydration stress. Transcriptome analysis revealed that Latrunculin A, an MF polymerization inhibitor, significantly suppressed the expression of actin and ABPs genes. Further analysis indicated that MF participates in the responses to desiccation in N. yezoensis by regulating plastid function, ROS levels, phosphorylation modification of proteins, Ca2+ signals and vesicle transport processes. Additionally, two MYB transcriptional factors were identified as being induced by regulating the MF cytoskeleton assembly. Finally, we developed a hypothesis concerning the regulation of the microfilament skeleton as a fundamental response to water loss in thalli of N. yezoensis. Our findings will enhance our understanding the adaption mechanisms of N. yezoensis to water stress and broaden our knowledge regarding the response of MF cytoskeleton to water stress. Furthermore, this research will provide valuable insights into the species distribution of intertidal zones.
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spelling doaj-art-ab53d6121e0a4c0db5c7b629f1fe131b2025-08-20T02:55:53ZengElsevierPlant Stress2667-064X2025-03-011510076210.1016/j.stress.2025.100762Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zoneJiqiang Yin0Ying Sun1Xinping Miao2Jiaxin Qu3Kunjie Zhang4Xue qing Han5Yichi Li6Jiahui Sun7Fanna Kong8College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, China; Dalian Marine Center, MNR, Dalian, Liaoning Province 116015, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, China; Corresponding author at: College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China.The microfilament (MF) cytoskeleton, present in all eukaryotic cells, is not only essential for fundamental cellular processes but also is important in sensing and transducing external signals in response to various developmental cues and abiotic stresses. Neopyropia yezoensis, a species of seaweed belonging to the Rhodophyta, is an important macroalga that thrives in the intertidal zone. However, it remains uncertain whether the MF cytoskeleton of seaweed contributes to adaption to desiccation and rehydration. In this study, we present for the first time the evidence regarding the role of MFs in the desiccation tolerance of N. yezoensis. The organization and arrangement of MFs were significantly influenced by variations in the water content within thallus cells. Desiccation of the thallus induced changes of many actin and actin binding proteins (ABPs) at transcriptional, translational and post-translational phosphorylation levels. Notably, nine phosphosites from four proteins (actin, formin, septin, and fascin) showed changes in phosphorylation conditions. This indicate that phosphorylation modification was involved in MFs response to desiccation and rehydration stress. Transcriptome analysis revealed that Latrunculin A, an MF polymerization inhibitor, significantly suppressed the expression of actin and ABPs genes. Further analysis indicated that MF participates in the responses to desiccation in N. yezoensis by regulating plastid function, ROS levels, phosphorylation modification of proteins, Ca2+ signals and vesicle transport processes. Additionally, two MYB transcriptional factors were identified as being induced by regulating the MF cytoskeleton assembly. Finally, we developed a hypothesis concerning the regulation of the microfilament skeleton as a fundamental response to water loss in thalli of N. yezoensis. Our findings will enhance our understanding the adaption mechanisms of N. yezoensis to water stress and broaden our knowledge regarding the response of MF cytoskeleton to water stress. Furthermore, this research will provide valuable insights into the species distribution of intertidal zones.http://www.sciencedirect.com/science/article/pii/S2667064X25000272Neopyropia yezoensisMicrofilament cytoskeletonDesiccation/rehydration stress
spellingShingle Jiqiang Yin
Ying Sun
Xinping Miao
Jiaxin Qu
Kunjie Zhang
Xue qing Han
Yichi Li
Jiahui Sun
Fanna Kong
Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
Plant Stress
Neopyropia yezoensis
Microfilament cytoskeleton
Desiccation/rehydration stress
title Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
title_full Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
title_fullStr Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
title_full_unstemmed Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
title_short Dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of Neopyropia yezoensis inhabiting the intertidal zone
title_sort dynamic changes and transcriptome analyses reveal the microfilament skeleton response to water stress in thalli of neopyropia yezoensis inhabiting the intertidal zone
topic Neopyropia yezoensis
Microfilament cytoskeleton
Desiccation/rehydration stress
url http://www.sciencedirect.com/science/article/pii/S2667064X25000272
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