Morphological Innovation Drives Sperm Release in Bryophytes

Author:

Zhang Xinxin1ORCID,Bian Ang2ORCID,Yang Junbo3,Liang Ye4,Zhang Zhe5,Yan Meng6,Yuan Siqi7,Zhang Qun7ORCID

Affiliation:

1. Institute of Botany Chinese Academy of Sciences Beijing 100093 China

2. College of Computer Science Sichuan University Chengdu 610065 China

3. Shenzhen Branch Guangdong Laboratory of Lingnan Modern Agriculture Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs Agricultural Genomics Institute at Shenzhen Chinese Academy of Agricultural Sciences Shenzhen Guangdong 518120 China

4. Core Facility of the State Key Laboratory of Membrane Biology Peking University Beijing 100871 China

5. Department of Mechanical and Aerospace Engineering The Hong Kong University of Science and Technology Clear Water Bay Hong Kong 999077 China

6. School of Life Science Hangzhou Institute for Advanced Study University of Chinese Academy of Sciences Hangzhou Zhejiang 310024 China

7. College of Life Sciences State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization Nanjing Agricultural University Nanjing 210095 China

Abstract

AbstractPlant movements for survival are nontrivial. Antheridia in the moss Physcomitrium patens (P. patens) use motion to eject sperm in the presence of water. However, the biological and mechanical mechanisms that actuate the process are unknown. Here, the burst of the antheridium of P. patens, triggered by water, results from elastic instability and is determined by an asymmetric change in cell geometry. The tension generated in jacket cell walls of antheridium arises from turgor pressure, and is further promoted when the inner walls of apex burst in hydration, causing water and cellular contents of apex quickly influx into sperm chamber. The outer walls of the jacket cells are strengthened by NAC transcription factor VNS4 and serve as key morphomechanical innovations to store hydrostatic energy in a confined space in P. patens. However, the antheridium in liverwort Marchantia polymorpha (M. polymorpha) adopts a different strategy for sperm release; like jacket cell outer walls of P. patens, the cells surrounding the antheridium of M. polymorpha appear to play a similar role in the storage of energy. Collectively, the work shows that plants have evolved different ingenious devices for sperm discharge and that morphological innovations can differ.

Funder

National Natural Science Foundation of China

China Postdoctoral Science Foundation

Key Technologies Research and Development Program

Publisher

Wiley

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