Stomatal dynamics are regulated by leaf hydraulic traits and guard cell anatomy in nine true mangrove species

doi:10.1016/j.pld.2024.02.003

Abstract

Abstract: Stomatal regulation is critical for mangroves to survive in the hyper-saline intertidal zone where water stress is severe and water availability is highly fluctuant. However, very little is known about the stomatal sensitivity to vapour pressure deficit (VPD) in mangroves, and its co-ordination with stomatal morphology and leaf hydraulic traits. We measured the stomatal response to a step increase in VPD in situ, stomatal anatomy, leaf hydraulic vulnerability and pressure-volume traits in nine true mangrove species of five families and collected the data of genome size. We aimed to answer two questions:(1) Does stomatal morphology influence stomatal dynamics in response to a high VPD in mangroves? with a consideration of possible influence of genome size on stomatal morphology; and (2) do leaf hydraulic traits influence stomatal sensitivity to VPD in mangroves? We found that the stomata of mangrove plants were highly sensitive to a step rise in VPD and the stomatal responses were directly affected by stomatal anatomy and hydraulic traits. Smaller, denser stomata was correlated with faster stomatal closure at high VPD across the species of Rhizophoraceae, and stomata size negatively and vein density positively correlated with genome size. Less negative leaf osmotic pressure at the full turgor (π_o) was related to higher operating steady-state stomatal conductance (g_s); and a higher leaf capacitance (C_leaf) and more embolism resistant leaf xylem were associated with slower stomatal responses to an increase in VPD. In addition, stomatal responsiveness to VPD was indirectly affected by leaf morphological traits, which were affected by site salinity and consequently leaf water status. Our results demonstrate that mangroves display a unique relationship between genome size, stomatal size and vein packing, and that stomatal responsiveness to VPD is regulated by leaf hydraulic traits and stomatal morphology. Our work provides a quantitative framework to better understand of stomatal regulation in mangroves in an environment with high salinity and dynamic water availability.

Key words: Stomatal temporal kinetics, Vapour-pressure deficit (VPD), Leaf water relations, Leaf hydraulic vulnerability, Leaf osmotic potential, Genome size

Ya-Dong Qie, Qi-Wei Zhang, Scott A. M. McAdam, Kun-Fang Cao. Stomatal dynamics are regulated by leaf hydraulic traits and guard cell anatomy in nine true mangrove species[J]. Plant Diversity, 2024, 46(03): 395-405.

References

[1] Agduma, A. R., Jiang, X., Liang, D. M., et al., 2022. Stem hydraulic traits are decoupled from leaf ecophysiological traits in mangroves in Southern Philippines. J. Plant Biol. 65, 389-401.
[2] Aritsara, A. N. A., Wang, S., Li, B. N., et al., 2022. Divergent leaf and fine root "pressure-volume relationships" across habitats with varying water availability. Plant Physiol. 190, 2246-2259.
[3] Bao, S. D., 2000. Soil and Agricultural Chemistry Analysis. China Agriculture Press, Beijing.
[4] Beaulieu, J. M., Leitch, I. J., Patel, S., et al., 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 179, 975-986.
[5] Beckett, H. A., Bryant, C., Neeman, T., et al., 2023. Plasticity in branch water relations and stem hydraulic vulnerability enhances hydraulic safety in mangroves growing along a salinity gradient. Plant Cell Environ. http://doi.org/https://doi.org/10.1111/pce.14764.
[6] Brodribb, T. J., Field, T. S., Jordan, G. J., 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol. 144, 1890-1898.
[7] Brodribb, T. J., Holbrook, N. M., 2003. Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol. 132, 2166-2173.
[8] Brodribb, T. J., McAdam, S. A., Jordan, G. J., et al., 2014. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc. Natl. Acad. Sci. U.S.A. 111, 14489-14493.
[9] Brodribb, T. J., McAdam, S. A., 2011. Passive origins of stomatal control in vascular plants. Science, 331, 1197985.
[10] Buckley, T. N., John, G. P., Scoffoni, C., et al., 2017. The sites of evaporation within leaves. Plant Physiol. 173, 1763-1782.
[11] Buckley, T. N., Mott, K. A., 2002. Stomatal water relations and the control of hydraulic supply and demand. Prog. Bot. 63, 309-325.
[12] Buckley, T. N., 2019. How do stomata respond to water status?New Phytol. 224, 21-36.
[13] Buckley, T. N., 2016. Stomatal responses to humidity:has the'black box'finally been opened?Plant Cell Environ. 39, 482-484.
[14] Buckley, T. N., 2005. The control of stomata by water balance. New Phytol. 168, 275-292.
[15] Cai, G. C., Carminati, A., Gleason, S. M., et al., 2023. Soil-plant hydraulics explain stomatal efficiency-safety tradeoff. Plant Cell Environ. 46, 3120-3127.
[16] Chen, X. Y., 2020. Relationship between Leaf Anatomical Structure and Photosynthetic Capacity of Mangrove Plants in Hainan. Guangxi University, Nanning, China.
[17] Choat, B., Brodribb, T. J., Brodersen, C. R., et al., 2018. Triggers of tree mortality under drought. Nature. 28, 531-539.
[18] Cowan, I. R., 1965. Transport of water in the soil-plant-atmosphere continuum. J. Appl. Ecol. 2, 221-239.
[19] Cowan, I. R., 1977. Stomatal behaviour and environment. Adv. Bot. Res. 4, 117-228.
[20] Darwin, F., 1898. Observations on stomata. Philos. Trans. R. Soc. Lond. B Biol. Sci. 190, 531-621.
[21] de Boer, H. J., Drake, P. L., Wendt, E., et al., 2016a. Apparent overinvestment in leaf venation relaxes leaf morphological constraints on photosynthesis in arid habitats. Plant Physiol. 172, 2286-2299.
[22] de Boer, H. J., Price, C. A., Wagner-Cremer, F., et al., 2016b. Optimal allocation of leaf epidermal area for gas exchange. New Phytol. 210, 1219-1228.
[23] Drake, P. L., Froend, R. H., Franks, P. J., 2013. Smaller, faster stomata:scaling of stomatal size, rate of response, and stomatal conductance. J. Exp. Bot. 64, 495-505.
[24] Duke, N. C., Ball, M. C., Ellison, J. C., 1998. Factors influencing biodiversity and distributional gradients in mangroves. Global Ecol. Biogeogr. Lett. 7, 27-47.
[25] Durand, M., Brendel, O., Bure, C., et al., 2019. Altered stomatal dynamics induced by changes in irradiance and vapour-pressure deficit under drought:impacts on the whole-plant transpiration efficiency of poplar genotypes. New Phytol. 222, 1789-1802.
[26] Elliott-Kingston, C., Haworth, M., Yearsley, J. M., et al., 2016. Does size matter?Atmospheric CO₂ may be a stronger driver of stomatal closing rate than stomatal size in taxa that diversified under low CO₂. Front. Plant Sci. 7, e1253.
[27] Fu, X. L., Meinzer, F. C., Woodruff, D. R., et al., 2019. Coordination and trade-offs between leaf and stem hydraulic traits and stomatal regulation along a spectrum of isohydry to anisohydry. Plant Cell Environ. 42, 2245-2258.
[28] Gauthey, A., Backes, D., Balland, J., et al., 2022. The role of hydraulic failure in a massive mangrove die-off event. Front. Plant Sci. 13, 822136.
[29] Gerardin, T., Douthe, C., Flexas, J., et al., 2018. Shade and drought growth conditions strongly impact dynamic responses of stomata to variations in irradiance in Nicotiana tabacum. Environ. Exp. Bot. 153, 188-197.
[30] Han, S. M., 2011. Study on Landscape Pattern Dynamics and Driving Forces in Mangroves Wetlands of Dongzhaigang Harbour, Hainan Province. Ph.D. thesis, Beijing Forest University, Beijing, China.
[31] He, Z. W., Feng, X., Chen, Q. P., et al., 2022. Evolution of coastal forests based on a full set of mangrove genomes. Nat. Ecol. Evol. 6, 738-1749.
[32] Henry, C., John, G. P., Pan, R. H., et al., 2019. A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nat. Commun. 10, 3398.
[33] Hu, M. J., Sun, W. H., Tsai, W. C., et al., 2020. Chromosome-scale assembly of the Kandelia obovata genome. Hortic. Res. 7, 75.
[34] Jalakas, P., Takahashi, Y., Waadt, R., et al., 2021. Molecular mechanisms of stomatal closure in response to rising vapour pressure deficit. New Phytol. 232, 468-475.
[35] Jiang, G. F., Goodale, U. M., Liu, Y. Y., et al., 2017. Salt management strategy defines the stem and leaf hydraulic characteristics of six mangrove tree species. Tree Physiol. 37, 389-401.
[36] Jiang, G. F., Li, S. Y., Li, Y. C., et al., 2022. Coordination of hydraulic thresholds across roots, stems, and leaves of two co-occurring mangrove species. Plant Physiol. 189, 2159-2174.
[37] Jiang, G. F., Li, S. Y., Dinnage, R., et al., 2023. Diverse mangroves deviate from other angiosperms in their genome size, leaf cell size and cell packing density relationships. Ann. Bot. 131, 347-360.
[38] Jiang, X., 2021. Xylem Hydraulic Structure and Function in Mangroves. Ph.D. thesis, Guangxi University, Nanning, China.
[39] Jiang, X., Choat, B., Zhang, Y. J., et al., 2021. Variation in xylem hydraulic structure and function of two mangrove species across a latitudinal gradient in Eastern Australia. Water. 13, 850.
[40] Lawson, T., Vialet-Chabrand, S., 2019. Speedy stomata, photosynthesis and plant water use efficiency. New Phytol. 221, 93-98.
[41] Leng, B., 2020. Transpriational Water Consumption and its Influencing Factors in Mangroves of Intertidal Zone. Ph.D. thesis, Guangxi University, Nanning, China.
[42] Martins, S. C. V., McAdam, S. A. M., Deans, R. M., et al., 2016. Stomatal dynamics are limited by leaf hydraulics in ferns and conifers:results from simultaneous measurements of liquid and vapour fluxes in leaves. Plant Cell Environ. 39, 694-705.
[43] Martin-StPaul, N., Delzon, S., Cochard, H., 2017. Plant resistance to drought depends on timely stomatal closure. Ecol. Lett. 20, 1437-1447.
[44] McAdam, S. A. M., Brodribb, T. J., 2015. The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol. 167, 833-843.
[45] McAdam, S. A. M., Brodribb, T. J., 2016. Linking turgor with ABA biosynthesis:implications for stomatal responses to vapor pressure deficit across land plants. Plant Physiol. 171, 2008-2016.
[46] McAusland, L., Vialet-Chabrand, S., Davey, P., et al., 2016. Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol. 211, 1209-1220.
[47] Meinzer, F. C., 1993. Stomata1 control of transpiration. Tree. 8, 289-294.
[48] Meinzer, F. C., Smith, D. D., Woodruff, D. R., et al., 2017. Stomatal kinetics and photosynthetic gas exchange along a continuum of isohydric to anisohydric regulation of plant water status. Plant Cell Environ. 40, 1618-1628.
[49] Peak, D., Mott, K. A., 2011. A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant Cell Environ. 34, 162-178.
[50] Raven, J. A., 2014. Speedy small stomata?J. Exp. Bot. 65, 1415-1424.
[51] Reef, R., Lovelock, C. E., 2015. Regulation of water balance in mangroves. Ann. Bot. 115, 385-395.
[52] Rockwell, F. E., Holbrook, N. M., Stroock, A. D., 2014. The competition between liquid and vapor transport in transpiring leaves. Plant Physiol. 164, 1741-1758.
[53] Rodriguez-Dominguez, C. M., Brodribb, T. J., 2020. Declining root water transport drives stomatal closure in olive under moderate water stress. New Phytol. 225, 126-134.
[54] Sack, L., Frole, K., 2006. Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees. Ecology. 87, 483-491.
[55] Sack, L., Holbrook, N. M., 2006. Leaf hydraulics. Annu. Rev. Plant Biol. 57, 361-381.
[56] Sack, L., Pasquet-Kok, J., Bartlett, M., 2011. Leaf pressure-volume curve parameters. PrometheusWiki. Available at:https://prometheusprotocols.net/function/water-relations/pressure-volume-curves/leaf-pressure-volume-curve-parameters.
[57] Scoffoni, C., Albuquerque, C., Brodersen, C. R., et al., 2017. Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiol. 173, 1197-1210.
[58] Scoffoni, C., McKown, A. D., Rawls, M., et al., 2012. Dynamics of leaf hydraulic conductance with water status:quantification and analysis of species differences under steady state. J. Exp. Bot. 63, 643-658.
[59] Simonin, K. A., Roddy, A. B., 2018. Genome downsizing, physiological novelty, and the global dominance of flowering plants. PLoS Biol. 16, e2003706.
[60] Skelton, R. P., Brodribb, T. J., McAdam, S. A., et al., 2017. Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance:evidence from an evergreen woodland. New Phytol. 215, 1399-1412.
[61] Skelton, R. P., Dawson, T. E., Thompson, S. E., et al., 2018. Low vulnerability to xylem embolism in leaves and stems of North American oaks. Plant Physiol. 177, 1066-1077.
[62] Sperry, J. S., 2000. Hydraulic constraints on plant gas exchange. Agric. For. Meteorol. 104, 13-23.
[63] Tardieu, F., 2016. Too many partners in root-shoot signals. Does hydraulics qualify as the only signal that feeds back over time for reliable stomatal control?New Phytol. 212, 954-963.
[64] Trueba, S., Pan, R. H., Scoffoni, C., et al., 2019. Thresholds for leaf damage due to dehydration:declines of hydraulic function, stomatal conductance and cellular integrity precede those for photochemistry. New Phytol. 223, 134-149.
[65] Tyree, M. T., Hammel, H. T., 1972. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J. Exp. Bot. 23, 267-282.
[66] Vialet-Chabrand, S., Dreyer, E., Brendel, O., 2013. Performance of a new dynamic model for predicting diurnal time courses of stomatal conductance at the leaf level. Plant Cell Environ. 36, 1529-1546.
[67] Xiong, D. L., Nadal, M., 2020. Linking water relations and hydraulics with photosynthesis. Plant J. 101, 800-815.