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Cai, S., Y. Huang, F. Chen, X. Zhang, E. Sessa, C. Zhao, D. B. Marchant, D. Xue, G. Chen, F. Dai, J. H. Leebens‐Mack, G. Zhang, S. Shabala, J. M. Christie, M. R. Blatt, E. Nevo, P. S. Soltis, D. E. Soltis, P. J. Franks, F. Wu, and Z. Chen. 2021. Evolution of rapid blue‐light response linked to explosive diversification of ferns in angiosperm forests. New Phytol 230:1201–1213. [View on publisher’s site]

Summary

Figure 1Light-induced stomatal responses in different green plants. (a) The topology of fern orders. Thetree was constructed with Brassicales and Selaginellales as outgroups. The number in parentheses represents the number of fern species in each order. (b, c) Stomatal aperture response to blue light (100 μmol m−2 s−1) in epidermal peels of leptosporangiate ferns (Nephrolepis exaltata, Polystichum proliferum, Microsorum pustulatum, Pellaea viridis, Adiantum fragrans, Cyathea cooperi, Lygodium microphyllum, Todea barbara, Ceratopteris richardi) compared with eusporangiate fern lineages (Angiopteris evecta, Equisetum hyemale, Psilotum nudum), as well as a reference lycophyte (Selaginella kraussiana) and a model angiosperm (Arabidopsis thaliana). The control represents the average value of stomatal aperture in the first 20 min, whereas blue-light treatment represents the stomatal aperture after 100 min blue-light treatment (n = 4 biological replicates with 30–50 stomata for each plant species; data are means ± SE; *, P < 0.05; **, P < 0.01). (d) Dose response of stomata to blue light in N. exaltata. Stomatal aperture was measured in response to 1, 10, 25, 50 and 100 μmol m−2 s−1 blue light (n = 4 biological replicates with 30–50 stomata; data are means ± SE). (e) Response of N. exaltata stomata to different light wavelengths. The light treatments include red (675 ± 25 nm, 250 μmol m−2 s−1), orange (593 ± 40 nm, 150 μmol m−2 s−1), green (527 ± 20 nm, 100 μmol m−2 s−1) and blue light (475 ± 25 nm, 100 μmol m−2 s−1) and UV-A (370 ± 36 nm, 75 μmol m−2 s−1). Four biological replicates with 30–50 stomata were used for each treatment; data are means ± SE.
Light-induced stomatal responses in different green plants. (a) The topology of fern orders. Thetree was constructed with Brassicales and Selaginellales as outgroups. The number in parentheses represents the number of fern species in each order. (b, c) Stomatal aperture response to blue light (100 μmol m−2 s−1) in epidermal peels of leptosporangiate ferns (Nephrolepis exaltata, Polystichum proliferum, Microsorum pustulatum, Pellaea viridis, Adiantum fragrans, Cyathea cooperi, Lygodium microphyllum, Todea barbara, Ceratopteris richardi) compared with eusporangiate fern lineages (Angiopteris evecta, Equisetum hyemale, Psilotum nudum), as well as a reference lycophyte (Selaginella kraussiana) and a model angiosperm (Arabidopsis thaliana). The control represents the average value of stomatal aperture in the first 20 min, whereas blue-light treatment represents the stomatal aperture after 100 min blue-light treatment (n = 4 biological replicates with 30–50 stomata for each plant species; data are means ± SE; *, P < 0.05; **, P < 0.01). (d) Dose response of stomata to blue light in N. exaltata. Stomatal aperture was measured in response to 1, 10, 25, 50 and 100 μmol m−2 s−1 blue light (n = 4 biological replicates with 30–50 stomata; data are means ± SE). (e) Response of N. exaltata stomata to different light wavelengths. The light treatments include red (675 ± 25 nm, 250 μmol m−2 s−1), orange (593 ± 40 nm, 150 μmol m−2 s−1), green (527 ± 20 nm, 100 μmol m−2 s−1) and blue light (475 ± 25 nm, 100 μmol m−2 s−1) and UV-A (370 ± 36 nm, 75 μmol m−2 s−1). Four biological replicates with 30–50 stomata were used for each treatment; data are means ± SE.

 

  • Ferns appear in the fossil record some 200 Myr before angiosperms. However, as angiosperm-dominated forest canopies emerged in the Cretaceous period there was an explosive diversification of modern (leptosporangiate) ferns, which thrived in low, blue-enhanced light beneath angiosperm canopies. A mechanistic explanation for this transformative event in the diversification of ferns has remained elusive.
  • We used physiological assays, transcriptome analysis and evolutionary bioinformatics to investigate a potential connection between the evolution of enhanced stomatal sensitivity to blue light in modern ferns and the rise of angiosperm-dominated forests in the geological record.
  • We demonstrate that members of the largest subclade of leptosporangiate ferns, Polypodiales, have significantly faster stomatal response to blue light than more ancient fern lineages and a representative angiosperm. We link this higher sensitivity to levels of differentially expressed genes in blue-light signaling, particularly in the cryptochrome (CRY) signaling pathway. Moreover, CRYs of the Polypodiales examined show gene duplication events between 212.9–196.9 and 164.4–151.8 Ma, when angiosperms were emerging, which are lacking in other major clades of extant land plants.
  • These findings suggest that evolution of stomatal blue-light sensitivity helped modern ferns exploit the shady habitat beneath angiosperm forest canopies, fueling their Cretaceous hyperdiversification.