Molecular basis of phenotypic plasticity in a marine ciliate

Author:

Pan Jiao12,Wang Yaohai1,Li Chao1,Zhang Simo3,Ye Zhiqiang4,Ni Jiahao1,Li Haichao1,Li Yichen1,Yue Hongwei1,Ruan Chenchen1,Zhao Dange1,Jiang Yujian1,Wu Xiaolin1,Shen Xiaopeng5,Zufall Rebecca A6,Zhang Yu7,Li Weiyi8,Lynch Michael9,Long Hongan12

Affiliation:

1. Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education), Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, Shandong 266003 , China

2. Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center , Qingdao, Shandong 266237 , China

3. Department of Biology, Indiana University , Bloomington, IN 47405 , United States

4. School of Life Sciences, Central China Normal University , Wuhan, Hubei 430079 , China

5. College of Life Sciences, Anhui Normal University , Wuhu, Anhui 241000 , China

6. Department of Biology and Biochemistry, University of Houston , Houston, TX 77204 , United States

7. School of Mathematics Science, Ocean University of China , Qingdao, Shandong Province 266000 , China

8. Department of Genetics, Stanford University School of Medicine , Stanford, CA 94305 , United States

9. Biodesign Center for Mechanisms of Evolution, Arizona State University , Tempe, AZ 85287 , United States

Abstract

Abstract Phenotypic plasticity, which involves phenotypic transformation in the absence of genetic change, may serve as a strategy for organisms to survive in complex and highly fluctuating environments. However, its reaction norm, molecular basis, and evolution remain unclear in most organisms, especially microbial eukaryotes. In this study, we explored these questions by investigating the reaction norm, regulation, and evolution of phenotypic plasticity in the cosmopolitan marine free-living ciliates Glauconema spp., which undergo significant phenotypic changes in response to food shortages. This study led to the de novo assembly of macronuclear genomes using long-read sequencing, identified hundreds of differentially expressed genes associated with phenotypic plasticity in different life stages, validated the function of two of these genes, and revealed that the reaction norm of body shape in response to food density follows a power-law distribution. Purifying selection may be the dominant evolutionary force acting on the genes associated with phenotypic plasticity, and the overall data support the hypothesis that phenotypic plasticity is a trait maintained by natural selection. This study provides novel insight into the developmental genetics of phenotypic plasticity in non-model unicellular eukaryotes and sheds light on the complexity and long evolutionary history of this important survival strategy.

Funder

National Science Foundation

National Institutes of Health

Postdoctoral Fellowship Program of CPSF

Taishan Scholars Program of Shandong Province, Shandong Province Natural Science Foundation

Laoshan Laboratory

National Natural Science Foundation of China

Publisher

Oxford University Press (OUP)

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