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Specialized herbivory in fossil leaves reveals convergent origins of nyctinasty

2023; Elsevier BV; Volume: 33; Issue: 4 Linguagem: Inglês

10.1016/j.cub.2022.12.043

1879-0445

Zhuo Feng, Qun Sui, Jiyuan Yang, Yun Guo, Stephen McLoughlin,

Plant and animal studies

Plants can move in various complex ways in response to external stimuli. 1 Chen J. Moreau C. Liu Y. Kawaguchi M. Hofer J. Ellis N. Chen R. Conserved genetic determinant of motor organ identity in Medicago truncatula and related legumes. Proc. Natl. Acad. Sci. USA. 2012; 109: 11723-11728https://doi.org/10.1073/pnas.1204566109 Crossref PubMed Scopus (50) Google Scholar ,2 Oikawa T. Ishimaru Y. Munemasa S. Takeuchi Y. Washiyama K. Hamamoto S. Yoshikawa N. Mutara Y. Uozumi N. Ueda M. channels regulate nyctinastic leaf opening in Samanea saman. Curr. Biol. 2018; 28: 2230-2238.e7https://doi.org/10.1016/j.cub.2018.05.042 Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar These mechanisms include responses to environmental triggers, such as tropic responses to light or gravity and nastic responses to humidity or contact. 3 Cortizo M. Laufs P. Genetic basis of the “sleeping leaves” revealed. Proc. Natl. Acad. Sci. USA. 2012; 109: 11474-11475https://doi.org/10.1073/pnas.1209532109 Crossref PubMed Scopus (11) Google Scholar Nyctinasty, the movements involving circadian rhythmic folding at night and opening at daytime of plant leaves or leaflets, has attracted the attention of scientists and the public for centuries. 4 Ueda M. Ishimaru Y. Takeuchi Y. Muraoka Y. Plant nyctinasty—who will decode the ‘Rosetta Stone’?. New Phytol. 2019; 223: 107-112https://doi.org/10.1111/nph.15717 Crossref PubMed Scopus (14) Google Scholar ,5 Yang G. Ishimaru Y. Hoshino S. Muraoka Y. Uozumi N. Ueda M. 12-Hydroxyjasmonic acid glucoside causes leaf-folding of Samanea saman through ROS accumulation. Sci. Rep. 2022; 12: 7232https://doi.org/10.1038/s41598-022-11414-2 Crossref PubMed Scopus (2) Google Scholar In his canonical work entitled The Power of Movement in Plants, Charles Darwin carried out pioneering observations to document the diverse range of movements in plants. 6 Darwin C. Darwin F. The Power of Movement in Plants. third thousand. John Murray, 1882 Google Scholar His systematic examination of plants showing “sleep [folding] movements of leaves” led him to conclude that the legume family (Fabaceae) includes many more nyctinastic species than all other families combined. 3 Cortizo M. Laufs P. Genetic basis of the “sleeping leaves” revealed. Proc. Natl. Acad. Sci. USA. 2012; 109: 11474-11475https://doi.org/10.1073/pnas.1209532109 Crossref PubMed Scopus (11) Google Scholar Darwin also found that a specialized motor organ, the pulvinus, is responsible for most sleep movements of plant leaves, although differential cell division and the hydrolysis of glycosides and phyllanthurinolactone also facilitate nyctinasty in some plants. 7 Ueda M. Nakamura Y. Chemical basis of plant leaf movement. Plant Cell Physiol. 2007; 48: 900-907https://doi.org/10.1093/pcp/pcm060 Crossref PubMed Scopus (46) Google Scholar ,8 Ueda M. Asano M. Sawai Y. Yamamura S. Leaf-movement factors of nyctinastic plant, Phyllanthus urinaria L.; the universal mechanism for the regulation of nyctinastic leaf-movement. Tetrahedron. 1999; 55: 5781-5792https://doi.org/10.1016/S0040-4020(99)00236-7 Crossref Scopus (27) Google Scholar However, the origin, evolutionary history, and functional benefits of foliar sleep movements remain ambiguous owing to the lack of fossil evidence for this process. Here, we document the first fossil evidence of foliar nyctinasty based on a symmetrical style of insect feeding damage (Folifenestra symmetrica isp. nov.) in gigantopterid seed-plant leaves from the upper Permian (∼259–252 Ma) of China. The pattern of insect damage indicates that the host leaves were attacked when mature but folded. Our finding reveals that foliar nyctinasty extends back to the late Paleozoic and evolved independently among various plant lineages.