Research Paper

Active stomatal control of Marsilea crenata, an amphibious fern, in response to CO2 and exogenous application of ABA

Tai-Chung Wu, Bai-Ling Lin, Wen-Yuan Kao

Published on: 02 September 2020

Page: 431 - 437

DOI: 10.6165/tai.2020.65.431

Abstract

Angiosperms have active stomatal control in response to rising CO2 and plant regulator abscisic acid (ABA). Whether ferns have similar response is controversial. To evaluate its stomatal response, we measured leaf photosynthetic gas exchange of Marsilea crenata (an amphibious fern), grown under full light and shaded condition, in response to variations in CO2 concentration ([CO2]) and exogenous application of ABA. The results showed that stomatal conductance (gs) of M. crenata significantly decreased while photosaturated photosynthetic rate (Amax) increased as [CO2] increased from 0 to 600 ppm, resulting in increments in water use efficiency (WUE). The reduction in gs when [CO2] was elevated from 400 to 800 ppm was more in leaves of full light-grown than those of shade-grown plants, however, the increment in Amax was similar. Leaves of M. crenata gradually closed stomata after 30 minutes of application of exogenous ABA, resulting in a 52.1 % reduction in gs and a 40 % in Amax, hence a 25 % increase of WUE. A more than two-fold increment of ABA contents was also measured in the leaves after the ABA application. This study showed that stomata of M. crenata do respond to the increase of ambient [CO2] from 0 to 600 ppm and to the ABA application, and the response to the elevated ambient [CO2] is affected by growth conditions.

Keyword: Active stomatal control, abscisic acid, CO2, Marsilea crenata, water use efficiency

Literature Cited

Brodribb, T.J., and S.A.M. McAdam. 2011. Passive origins of stomatal control in vascular plants. Science 331(6017): 582.
DOI: 10.1126/science.1197985View Article Google Scholar

Brodribb, T.J., and S.A.M. McAdam. 2013. Unique responsiveness of angiosperm stomata to elevated CO2 explained by calcium signalling. PLOS ONE 8(11): e82057.
DOI: 10.1371/journal.pone.0082057View Article Google Scholar

Brodribb, T.J., S.A. M. McAdam, G.J. Jordan, and T.S. Feild. 2009. Evolution of stomatal responsiveness to CO2 and optimization of water?use efficiency among land plants. New Phytol. 183(3): 839–847.
DOI: 10.1111/j.1469-8137.2009.02844.xView Article Google Scholar

Bunce, J.A. 2004. Carbon dioxide effects on stomatal responses to the environment and water use by crops under field conditions. Oecologia 140(1): 1?10.
DOI: 10.1007/s00442-003-1401-6View Article Google Scholar

Cai, S., G. Chen, Y. Wang, Y. Huang, D.B. Marchant, Y. Wang, Q. Yang, F. Dai, A. Hills, P.J. Franks, E. Nevo, D.E. Soltis, P.S. Soltis, E. Sessa, P.G. Wolf, D. Xue, G. Zhang, B.J. Pogson, M.R. Blatt, and Z.-H. Chen. 2017. Evolutionary Conservation of ABA Signaling for Stomatal Closure. Plant Physiol. 174(2): 732?747.
DOI: 10.1104/pp.16.01848View Article Google Scholar

Centritto, M., M.E. Lucas, and P.G. Jarvis. 2002. Gas exchange, biomass, whole-plant water-use efficiency and water uptake of peach (Prunus persica) seedlings in response to elevated carbon dioxide concentration and water availability. Tree Physiol. 22(10): 699?706.
DOI: 10.1093/treephys/22.10.699View Article Google Scholar

Chater, C., Y. Kamisugi, M. Movahedi, A. Fleming, Andrew C. Cuming, Julie E. Gray, and David J. Beerling. 2011. Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr. Biol. 21(12): 1025?1029.
DOI: 10.1016/j.cub.2011.04.032View Article Google Scholar

Creese, C., S. Oberbauer, P. Rundel, and L. Sack. 2014. Are fern stomatal responses to different stimuli coordinated? Testing responses to light, vapor pressure deficit, and CO2 for diverse species grown under contrasting irradiances. New Phytol. 204(1): 92?104.
DOI: 10.1111/nph.12922View Article Google Scholar

Das, V.S.R., I.M. Rao, and A.S. Raghavendra. 1976. Reversal of abscisic acid induced stomatal closure by benzyl adenine. New Phytol. 76(3): 449?452.
DOI: 10.1111/j.1469-8137.1976.tb01480.xView Article Google Scholar

Darwin, F. 1898. Observations on stomata. Proc. R. Soc. Lond. 63(389-400): 413?417.
DOI: 10.1098/rspl.1898.0053View Article Google Scholar

Doi, M., and K.I. Shimazaki. 2008. The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiol. 147(2): 922?930.
DOI: 10.1104/pp.108.118950View Article Google Scholar

Doi, M., M. Wada, and K. Shimazaki. 2006. The fern Adiantum capillus-veneris lacks stomatal responses to blue light. Plant Cell Physiol. 47(6): 748.
DOI: 10.1093/pcp/pcj048View Article Google Scholar

Drake, B.G., M.A. Gonz?lez-Meler, and S.P. Long. 1997. More efficient plants: A consequence of rising atmospheric CO2? Annu. Rev. Plant Physiol. Plant Mol. Biol. 48(1): 609?639.
DOI: 10.1146/annurev.arplant.48.1.609View Article Google Scholar

Franks, P.J. 2013. Passive and active stomatal control: either or both? New Phytol. 198(2): 325?327.
DOI: 10.1111/nph.12228View Article Google Scholar

Franks, P.J., and Z.J. Britton-Harper. 2016. No evidence of general CO2 insensitivity in ferns: one stomatal control mechanism for all land plants? New Phytol. 211(3): 819?827.
DOI: 10.1111/nph.14020View Article Google Scholar

Franks, P.J., and G.D. Farquhar. 2001. The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol. 125(2): 935?942.
DOI: 10.1104/pp.125.2.935View Article Google Scholar

Guo, J.M., and C.M. Trotter. 2006. Estimating photosynthetic light?use efficiency using the photochemical reflectance index: the effects of short?term exposure to elevated CO2 and low temperature. Int. J. Remote Sens. 27(20): 4677?4684.
DOI: 10.1080/01431160500165997View Article Google Scholar

Hartung, W. 2010. The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct. Plant Biol. 37(9): 806?812.
DOI: 10.1071/FP10058View Article Google Scholar

Haworth, M., C. Elliott-Kingston, and J.C. McElwain. 2013. Co-ordination of physiological and morphological responses of stomata to elevated [CO2] in vascular plants. Oecologia 171(1): 71?82.
DOI: 10.1007/s00442-012-2406-9View Article Google Scholar

Hikosaka, K., T. Yamano, H. Nagashima, and T. Hirose. 2003. Light-acquisition and use of individuals as influenced by elevated CO2 in even-aged monospecific stands of Chenopodium album. Funct. Ecol. 17(6): 786?795.
DOI: 10.1111/j.1365-2435.2003.00793.xView Article Google Scholar

H?rak, H., H. Kollist, and E. Merilo. 2017. Fern stomatal responses to ABA and CO2 depend on species and growth conditions. Plant Physiol. 174(2): 672?679.
DOI: 10.1104/pp.17.00120View Article Google Scholar

Huang, Y.-C. 2015. Leaf stomatal response to blue light and CO2 concentration in six fern species. Master Thesis. NTU, Taipei, Taiwan.

Hurng, W.P., H.S. Lur, C.-K. Liao, and C.H. Kao. 1994. Role of abscisic acid, ethylene and polyamines in flooding-promoted senescence of tobacco leaves. J. Plant Physiol. 143(1): 102?105.
DOI: 10.1016/S0176-1617(11)82104-8View Article Google Scholar

Keeley, J.E. 1983. Crassulacean acid metabolism in the seasonally submerged aquatic Isoetes howellii. Oecologia 58(1): 57–62.
DOI: 10.1007/BF00384542View Article Google Scholar

Lin, B.L., and W.J. Yang. 1999. Blue light and abscisic acid independently induce heterophyllous switch in Marsilea quadrifolia. Plant Physiol. 119(2):429–434.
DOI: 10.1104/pp.119.2.429View Article Google Scholar

Liu, B.L.L. 1984. Abscisic acid induces land form characteristics in Marsilea quadrifolia L. Am. J. Bot. 71(5): 638–644.
DOI: 10.2307/2443360View Article Google Scholar

Maherali, H., H.B. Johnson, and R.B. Jackson. 2003. Stomatal sensitivity to vapour pressure difference over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ. 26(8): 1297–1306.
DOI: 10.1046/j.1365-3040.2003.01054.xView Article Google Scholar

McAdam, S.A.M., and T.J. Brodribb. 2012. Stomatal innovation and the rise of seed plants. Ecol. Lett. 15(1): 1–8.
DOI: 10.1111/j.1461-0248.2011.01700.xView Article Google Scholar

McAdam, S.A.M., and T.J. Brodribb. 2014. Separating active and passive influences on stomatal control of transpiration. Plant Physiol. 164(4): 1578–1586.
DOI: 10.1104/pp.113.231944View Article Google Scholar

McAdam, S.A.M. and T.J. Brodribb. 2015. The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol. 167(3): 833–843
DOI: 10.1104/pp.114.252940View Article Google Scholar

McAdam, S.A.M, F.C. Sussmilch and T.J. Brodribb. 2016. Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant Cell Environ. 39(3): 485–491.
DOI: 10.1111/pce.12633View Article Google Scholar

Ruszala, E.M., D.J. Beerling, P.J. Franks, C. Chater, S.A. Casson, J.E. Gray, and A.M. Hetherington. 2011. Land plants acquired active stomatal control early in their evolutionary history. Curr. Biol. 21(12): 1030?1035.
DOI: 10.1016/j.cub.2011.04.044View Article Google Scholar

Shimazaki, K., M. Doi, S.M. Assmann, and T. Kinoshita. 2007. Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58(1): 219?247.
DOI: 10.1146/annurev.arplant.57.032905.105434View Article Google Scholar

Snaith, P.J., and T.A. Mansfield. 1982. Stomatal sensitivity to abscisic acid: can it be defined? Plant Cell Environ. 5(4): 309?311.
DOI: 10.1111/1365-3040.ep11572699View Article Google Scholar

Soni, D.K., S. Ranjan, R. Singh, P.B. Khare, U.V. Pathre, and P.A. Shirke. 2012. Photosynthetic characteristics and the response of stomata to environmental determinants and ABA in Selaginella bryopteris, a resurrection spike moss species. Plant Sci. 191-192: 43?52.
DOI: 10.1016/j.plantsci.2012.04.011View Article Google Scholar

Talbott, L.D., A. Srivastava, and E. Zeiger. 1996. Stomata from growth-chamber-grown Vicia faba have an enhanced sensitivity to CO2. Plant Cell Environ. 19(10): 1188?1194.
DOI: 10.1111/j.1365-3040.1996.tb00434.xView Article Google Scholar

Tardieu, F., and W.J. Davies. 1992. Stomatal response to abscisic acid is a function of current plant water status. Plant Physiol. 98(2): 540?545.
DOI: 10.1104/pp.98.2.540View Article Google Scholar

Tomimatsu, H., A. Iio, M. Adachi, L.-G. Saw, C. Fletcher, and Y. Tang. 2014. High CO2 concentration increases relative leaf carbon gain under dynamic light in Dipterocarpus sublamellatus seedlings in a tropical rain forest, Malaysia. Tree Physiol. 34(9): 944?954.
DOI: 10.1093/treephys/tpu066View Article Google Scholar

Wong, S.C. and C.S. Hew. 1976. Diffusive resistance, titratable acidity, and CO2 fixation in two tropical epiphytic ferns. Am. Fern J. 66(4): 121?124.
DOI: 10.2307/1546463View Article Google Scholar

Wu, T.C., and W.Y. Kao. 2009. The function of trichomes of an amphibious fern, Marsilea quadrifolia. Am. Fern J. 99(4): 323?333.
DOI: 10.1640/0002-8444-99.4.323View Article Google Scholar

Wullschleger, S.D., C.A. Gunderson, P.J. Hanson, K.B. Wilson, and R.J. Norby. 2002. Sensitivity of stomatal and canopy conductance to elevated CO2 concentration-interacting variables and perspectives of scale. New Phytol. 153(3): 485?496.
DOI: 10.1046/j.0028-646X.2001.00333.xView Article Google Scholar