journal article·2024-05Open access

Morphological Innovation Drives Sperm Release in Bryophytes

Xinxin Zhang, Ang Bian, Junbo Yang, Ye Liang, Zhe Zhang, Meng Yan, Siqi Yuan, Qun Zhang

Advanced Science· Volume 11· Issue 20

Abstract

Abstract Plant 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.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Plant Molecular Biology Research · Plant and Biological Electrophysiology Studies · Bryophyte Studies and Records

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Institute of Botany Chinese Academy of Sciences Beijing 100093 China

College of Computer Science Sichuan University Chengdu 610065 China

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

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

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

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

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

Funding

National Natural Science Foundation of China · China Postdoctoral Science Foundation · Key Technologies Research and Development Program

References (89)

Show source-provided references
1. 10.1016/j.cell.2016.05.00210.1016/j.cell.2016.05.002 ↗
2. 10.1126/science.121598510.1126/science.1215985 ↗
3. 10.1038/435164a10.1038/435164a ↗
4. 10.1126/science.130.3374.504.a10.1126/science.130.3374.504.a ↗
5. 10.1126/science.140.3572.123610.1126/science.140.3572.1236 ↗
6. 10.1038/nature0318510.1038/nature03185 ↗
7. 10.1073/pnas.190498411610.1073/pnas.1904984116 ↗
8. 10.1126/science.110797610.1126/science.1107976 ↗
9. 10.1016/j.gde.2018.04.00710.1016/j.gde.2018.04.007 ↗
10. Dyer A. F. · 1984
11. 10.1146/annurev.arplant.50.1.16310.1146/annurev.arplant.50.1.163 ↗
12. 10.1017/CBO978051162683810.1017/CBO9780511626838 ↗
13. 10.1017/CBO978051175480710.1017/CBO9780511754807 ↗
14. 10.2307/130840110.2307/1308401 ↗
15. 10.1080/2001359109920910.1080/20013591099209 ↗
16. 10.1111/tpj.1350110.1111/tpj.13501 ↗
17. 10.1105/tpc.19.0082810.1105/tpc.19.00828 ↗
18. 10.1098/rspb.1942.001210.1098/rspb.1942.0012 ↗
19. 10.1098/rstb.2016.049410.1098/rstb.2016.0494 ↗
20. 10.1104/pp.113.21402310.1104/pp.113.214023 ↗
21. Cronberg N. · Bryology in the New Millennium · 2008 · 347
22. 10.1093/plphys/kiab42610.1093/plphys/kiab426 ↗
23. 10.1111/jmi.1289510.1111/jmi.12895 ↗
24. 10.1111/j.1469-8137.2012.04329.x10.1111/j.1469-8137.2012.04329.x ↗
25. 10.1093/jxb/err01410.1093/jxb/err014 ↗
26. 10.1105/tpc.105.03600410.1105/tpc.105.036004 ↗
27. 10.1105/tpc.106.04639110.1105/tpc.106.046391 ↗
28. 10.1002/j.1537-2197.1977.tb07608.x10.1002/j.1537-2197.1977.tb07608.x ↗
29. 10.1111/j.1365-313X.2008.03633.x10.1111/j.1365-313X.2008.03633.x ↗
30. 10.3389/fpls.2015.0028810.3389/fpls.2015.00288 ↗
31. 10.1111/nph.1793810.1111/nph.17938 ↗
32. 10.1038/s41477-017-0082-910.1038/s41477-017-0082-9 ↗
33. 10.1111/tpj.1394010.1111/tpj.13940 ↗
34. 10.1126/science.124841710.1126/science.1248417 ↗
35. 10.1105/tpc.109.07227210.1105/tpc.109.072272 ↗
36. 10.1016/bs.mcb.2014.10.00610.1016/bs.mcb.2014.10.006 ↗
37. 10.1111/j.1365-313X.2011.04649.x10.1111/j.1365-313X.2011.04649.x ↗
38. 10.1126/sciadv.abc929410.1126/sciadv.abc9294 ↗
39. 10.1093/plcell/koaa04910.1093/plcell/koaa049 ↗
40. 10.1126/science.aaz510310.1126/science.aaz5103 ↗
41. 10.1016/j.pbi.2008.03.00610.1016/j.pbi.2008.03.006 ↗
42. 10.1016/j.cub.2015.05.02210.1016/j.cub.2015.05.022 ↗
43. 10.1016/j.tplants.2007.04.00110.1016/j.tplants.2007.04.001 ↗
44. Zhang X. · Plant Physiol. · 2023 · 1 · 603
45. 10.1105/tpc.106.04704310.1105/tpc.106.047043 ↗
46. 10.1007/BF0019300410.1007/BF00193004 ↗
47. 10.1111/j.1469-8137.1975.tb02617.x10.1111/j.1469-8137.1975.tb02617.x ↗
48. Sullivant W. S. · 1865
49. Gradstein S. R. · 2011
50. Lee G. E. · 2021
51. 10.1007/s00606-011-0498-z10.1007/s00606-011-0498-z ↗
52. 10.1086/32847810.1086/328478 ↗
53. Smith A. J. E. · 1990
54. Goffinet B. · Bryophyte Biology · 2009 · 2 · 55
55. 10.1093/pcp/pcw00510.1093/pcp/pcw005 ↗
56. 10.1016/j.cub.2019.10.00410.1016/j.cub.2019.10.004 ↗
57. 10.1111/nph.1613210.1111/nph.16132 ↗
58. 10.1016/j.cub.2020.05.08110.1016/j.cub.2020.05.081 ↗
59. 10.1016/j.pbi.2018.02.00610.1016/j.pbi.2018.02.006 ↗
60. 10.1098/rstb.2000.061510.1098/rstb.2000.0615 ↗
61. 10.1098/rstb.2011.025210.1098/rstb.2011.0252 ↗
62. 10.1038/nature0188410.1038/nature01884 ↗
63. 10.1126/science.115064610.1126/science.1150646 ↗
64. Cavers F. · Knowledge · 1910 · 7 · 294
65. 10.1104/pp.17.0071910.1104/pp.17.00719 ↗
66. 10.1093/pcp/pcv19210.1093/pcp/pcv192 ↗
67. 10.1111/j.1525-142X.2008.00271.x10.1111/j.1525-142X.2008.00271.x ↗
68. 10.1055/s-2002-3544010.1055/s-2002-35440 ↗
69. 10.1016/j.cell.2017.09.03010.1016/j.cell.2017.09.030 ↗
70. 10.1371/journal.pone.007735610.1371/journal.pone.0077356 ↗
71. 10.1242/dev.0064410.1242/dev.00644 ↗
72. 10.1016/j.cell.2009.12.02310.1016/j.cell.2009.12.023 ↗
73. 10.1023/A:100649630816010.1023/A:1006496308160 ↗
74. 10.1093/plphys/kiab57310.1093/plphys/kiab573 ↗
75. 10.1093/pcp/pcw20110.1093/pcp/pcw201 ↗
76. 10.1093/pcp/pcn08510.1093/pcp/pcn085 ↗
77. 10.1186/s13007-017-0186-210.1186/s13007-017-0186-2 ↗
78. 10.1016/j.carres.2008.11.01010.1016/j.carres.2008.11.010 ↗
79. 10.1038/nmeth.201910.1038/nmeth.2019 ↗
80. 10.1016/j.bspc.2021.10290310.1016/j.bspc.2021.102903 ↗
81. 10.1038/nmeth.331710.1038/nmeth.3317 ↗
82. 10.1093/gigascience/giab00810.1093/gigascience/giab008 ↗
83. 10.1093/bioinformatics/btp61610.1093/bioinformatics/btp616 ↗
84. 10.1038/nbt.312210.1038/nbt.3122 ↗
85. 10.1093/molbev/mst01010.1093/molbev/mst010 ↗
86. 10.1093/bioinformatics/btp34810.1093/bioinformatics/btp348 ↗
87. 10.1093/bioinformatics/btu03310.1093/bioinformatics/btu033 ↗
88. 10.1093/nar/gkab30110.1093/nar/gkab301 ↗
89. 10.1016/j.molp.2020.06.00910.1016/j.molp.2020.06.009 ↗