Abstract
This work aimed to evaluate the effects of lower water levels on leaf intercellular spaces and to assess their relations with the gas exchange, anatomy, and growth of Sorghum bicolor. Experiments were conducted in a greenhouse, in which plants were subjected to three water conditions (ten replicates, n = 30): well-irrigated, decreased irrigation, and limited irrigation. Lower water levels had no significant effect on the growth of S. bicolor but increased the biomass of the roots. Moreover, the number of leaves, leaf area, and leaf size as well as the chlorophyll content were not affected by lower water levels, and no significant changes were detected for whole plant photosynthesis, transpiration, or stomatal conductance. The water content of the plants and the water potential remained unchanged. However, compared with other treatments, the decreased irrigation decreased water loss and increased the water retention. Lower water levels increased the intercellular CO2 percentage, mesophyll area, and proportion of stomatal cavities and promoted minor changes in leaf tissue and stomatal traits. The increased stomatal cavities provided higher CO2 uptake and prevented excessive water loss. Thus, modifications to the intercellular spaces promoted conditions to avoid excessive water loss while concurrently improving CO2 uptake, which are important traits for drought-tolerant plants.
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Data availability
The data supporting the findings of this study are available from the corresponding author, Fabricio José Pereira, upon request.
References
Abdallah MB, Trupiano D, Polzella A, Zio E, Sassi M, Scaloni A, Scippa GS (2018) Unraveling physiological, biochemical and molecular mechanisms involved in olive (Olea europaea L. cv. Chétoui) tolerance to drought and salt stresses. J Plant Physiol 220:83–95. https://doi.org/10.1016/j.jplph.2017.10.009
Alberts B, Bray D, Hopkin K, Johnson A, Lewis J, Raff M, Walter P (2015) Essential cell biology. Garland Science
Allen LH, Kakani VG, Vu JCV, Boote KJ (2011) Elevated CO2 increases water use efficiency by sustaining photosynthesis of water-limited maize and sorghum. J Plant Physiol 168:1909–1918. https://doi.org/10.1016/j.jplph.2011.05.005
Anupama A, Bhugra S, Lall B, Chaudhury S, Chugh A (2019) Morphological, transcriptomic and proteomic responses of contrasting rice genotypes towards drought stress. Environ Exp Bot 166:103795. https://doi.org/10.1016/j.envexpbot.2019.06.008
Bhargava S, Paranjpe S (2004) Genotypic variation in the photosynthetic competence of Sorghum bicolor seedlings subjected to polyethylene glycol-mediated drought stress. J Plant Physiol 161:125–129. https://doi.org/10.1078/0176-1617-01126
Buckley TN, John GP, Scoffoni C, Sack L (2017) The sites of evaporation within leaves. Plant Physiol 173:1763–1782. https://doi.org/10.1104/pp.16.01605
Buckley TN (2019) How do stomata respond to water status? New Phytol 224:21–36. https://doi.org/10.1111/nph.15899
Cechin I (1998) Photosynthesis and chlorophyll fluorescence in two hybrids of sorghum under different nitrogen and water regimes. Photosynthetica 35:233–240. https://doi.org/10.1023/A:1006910823378
Chartzoulakis K, Patakas A, Kofidis G, Bosabalidis A, Nastou A (2002) Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars. Sci Hort 95:39–50. https://doi.org/10.1016/S0304-4238(02)00016-X
Clauw P, Coppens F, Beuf K, Dhondt S, Van Daele T, Maleux K, Inzé D (2015) Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiol 167:800–816. https://doi.org/10.1104/pp.114.254284
Cruz YC, Scarpa ALM, Pereira MP, Castro EM, Pereira FJ (2019) Growth of Typha domingensis as related to leaf physiological and anatomical modifications under drought conditions. Acta Physiol Plant 41:64. https://doi.org/10.1007/s11738-019-2858-1
Díaz AS, Aguiar GM, Pereira MP, Castro EM, Magalhães PC, Pereira FJ (2018) Aerenchyma development in different root zones of maize genotypes under water limitation and different phosphorus nutrition. Biol Plant 62:561–568. https://doi.org/10.1007/s10535-018-0773-8
Drobnitch ST, Comas LH, Flynn N, Ibarra CJ, Barton RW, Wenz JP, Person T, Bushey J, Jahn CE, Gleason SM (2021) Drought-induced root pressure in Sorghum bicolor. Front Plant Sci 12:571072. https://doi.org/10.3389/fpls.2021.571072
Earl HJ (2002) Stomatal and non-stomatal restrictions to carbon assimilation in soybean (Glycine max) lines differing in water use efficiency. Environ Exp Bot 48:237–246. https://doi.org/10.1016/S0098-8472(02)00041-2
Engineer CB, Ghassemian M, Anderson JC, Peck SC, Hu H, Schroeder JI (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature 513:246–250. https://doi.org/10.1038/nature13452
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Gleason SM, Cooper M, Wiggans DR, Bliss CA, Romay MC, Gore MA, Mickelbart MV, Topp CN, Zhang H, DeJonge KC, Comas LH (2019) Stomatal conductance, xylem water transport, and root traits underpin improved performance under drought and well-watered conditions across a diverse panel of maize inbred lines. Field Crops Res 234:119–128. https://doi.org/10.1016/j.fcr.2019.02.001
Gorthi A, Volenec JJ, Welp LR (2019) Stomatal response in soybean during drought improves leaf-scale and field-scale water use efficiencies. Agric For Meteorol 276:107629. https://doi.org/10.1016/j.agrformet.2019.107629
Guha A, Chhajed SS, Choudhary S, Sunny R, Jansen S, Barua D (2018) Hydraulic anatomy affects genotypic variation in plant water use and shows differential organ specific plasticity to drought in Sorghum bicolor. Environ Exp Bot 156:25–37. https://doi.org/10.1016/j.envexpbot.2018.08.025
Guo Y, Hu M, Liu LL, Yao W, Zhang MQ (2019) Activities of key enzymes in the C4 pathway and anatomy of sugarcane infected by Leifsonia xyli subsp. xyli. J Appl Microbiol 127:1790–1800. https://doi.org/10.1111/jam.14444
He J, Du YL, Wang T, Turner NC, Yang RP, Jin Y, Xi Y, Zhang C, Cui T, Fang XW, Li FM (2017) Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought. Agric Water Manag 179:236–245. https://doi.org/10.1016/j.agwat.2016.07.008
Hsie BS, Mendes KR, Antunes WC, Endres L, Campos MLO, Souza FC, Santos ND, Singh B, Arruda ECP, Pompelli MF (2015) Jatropha curcas L. (Euphorbiaceae) modulates stomatal traits in response to leaf-to-air vapor pressure deficit. Biomass Bioenergy 81:273–281. https://doi.org/10.1016/j.biombioe.2015.07.014
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:1–34
Hughes J, Hepworth C, Dutton C, Dunn JA, Hunt L, Stephens J, Waugh R, Cameron DD, Gray JE (2017) Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol 174:776–787. https://doi.org/10.1104/pp.16.01844
Impa SM, Perumal R, Bean SR, Sunoj VJ, Jagadish SK (2019) Water deficit and heat stress induced alterations in grain physico-chemical characteristics and micronutrient composition in field grown grain sorghum. J Cereal Sci 86:124–131. https://doi.org/10.1016/j.jcs.2019.01.013
Jarman PD (1974) The diffusion of carbon dioxide and water vapour through stomata. J Exp Bot 25:927–936. https://doi.org/10.1093/jxb/25.5.927
Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York
Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San Diego https://udspace.udel.edu/handle/19716/2830
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570. https://doi.org/10.1104/pp.114.237107
Lavinsky AO, Magalhães PC, Ávila RG, Diniz MM, Souza TC (2015) Partitioning between primary and secondary metabolism of carbon allocated to roots in four maize genotypes under water deficit and its effects on productivity. Crop J 3:379–386. https://doi.org/10.1016/j.cj.2015.04.008
Lawson T, Vialet-Chabrand S (2019) Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 221:93–98. https://doi.org/10.1111/nph.15330
Li X, Shi W, Broughton K, Smith R, Sharwood R, Payton P, Tissue DT (2020) Impacts of growth temperature, water deficit and heatwaves on carbon assimilation and growth of cotton plants (Gossypium hirsutum L.). Environ Exp Bot 179:104204. https://doi.org/10.1016/j.envexpbot.2020.104204
Liu B, Liang J, Tang G, Wang X, Liu F, Zhao D (2019) Drought stress affects on growth, water use efficiency, gas exchange and chlorophyll fluorescence of Juglans rootstocks. Sci Hort 250:230–235. https://doi.org/10.1016/j.scienta.2019.02.056
Luo L, Xia H, Lu B-R (2019) Editorial: crop breeding for drought resistance. Front Plant Sci 10:314. https://doi.org/10.3389/fpls.2019.00314
Melo HC, Castro EM, Soares AM, Melo LA, Alves JD (2007) Alterações anatômicas e fisiológicas em Setaria anceps Stapf ex Massey e Paspalum paniculatum L. sob condições de déficit hídrico. Hoehnea 34:145–153. https://doi.org/10.1590/S2236-89062007000200003
Mcausland L, Vialet-Chabrand S, Davey P, Baker NR, Brendel O, Lawson T (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211:1209–1220. https://doi.org/10.1111/nph.14000
Monson RK (1999) The origins of C4 genes and evolutionary pattern in the C4 metabolic phenotype. C4 Plant biology. Academic Press, USA, pp 377–410
Moroke TS, Schwartz RC, Brown KW, Juo ASR (2011) Water use efficiency of dryland cowpea, sorghum and sunflower under reduced tillage. Soil Tillage Res 112:76–84. https://doi.org/10.1016/j.still.2010.11.008
Ni XL, Meng Y, Zheng SS, Liu WZ (2014) Programmed cell death during aerenchyma formation in Typha angustifolia leaves. Aquat Bot 113:8–18. https://doi.org/10.1016/j.aquabot.2013.10.004
Ogbaga CC, Amir M, Bano H, Chater CC, Jellason NP (2020) Clarity on frequently asked questions about drought measurements in plant physiology. Scientific African 8:e00405. https://doi.org/10.1016/j.sciaf.2020.e00405
Özyiğit İİ, Akinci Ş (2009) Effects of some stress factors (aluminum, cadmium and drought) on stomata of Roman nettle (Urtica pilulifera L.). Not Bot Horti Agrobot Cluj-Napoca 37:108–115. https://doi.org/10.15835/nbha3713191
Pengelly JJL, Kwasny S, Bala S, Evans JR, Voznesenskaya EV, Koteyeva NK, Edwards GE, Furbank RT, Von Caemmerer S (2011) Functional analysis of corn husk photosynthesis. Plant Physiol 156:503–513. https://doi.org/10.1104/pp.111.176495
Santos KR, Pereira MP, Ferreira ACG, Almeida Rodrigues LC, Castro EM, Corrêa FF, Pereira FJ (2015) Typha domingensis Pers. Growth responses to leaf anatomy and photosynthesis as influenced by phosphorus. Aquat Bot 122:47–53. https://doi.org/10.1016/j.aquabot.2015.01.007
Scholander PF, Bradstrect ED, Hemmingsen EA, Hammel HT (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148:339–148. https://doi.org/10.1126/science.148.3668.339
Segatto FB, Bisognin DA, Benedetti M, Costa LC, Rampelotto MV, Nicoloso FT (2004) A technique for the anatomical study of potato leaf epidermis. Cienc Rural 34:1597–1601. https://doi.org/10.1590/S0103-84782004000500042
Silva EC, Nogueira RJ, Vale FH, Araújo FPD, Pimenta MA (2009) Stomatal changes induced by intermittent drought in four umbu tree genotypes. Braz J Plant Physiol 21:33–42. https://doi.org/10.1590/S1677-04202009000100005
Souza TC, Magalhães PC, Castro EM, Duarte VP, Lavinsky AO (2016) Corn root morphoanatomy at different development stages and yield under water stress. Pesq Agropec Bras 51:330–339. https://doi.org/10.1590/S0100-204X2016000400005
Song L, Jin J (2020) Improving CERES-Maize for simulating maize growth and yield under water stress conditions. Eur J Agron 117:126072. https://doi.org/10.1016/j.eja.2020.126072
Stout DG, Simpson GM (1978) Drought resistance of Sorghum bicolor. 1. Drought avoidance mechanisms related to leaf water status. Can J Plant Sci 58:213–224. https://doi.org/10.4141/cjps78-031
Sutka MR, Manure ME, Vitali VA, Micheletto S, Amodeo G (2016) Evidence for the involvement of hydraulic root or shoot adjustments as mechanisms underlying water deficit tolerance in two Sorghum bicolor genotypes. J Plant Physiol 192:13–20. https://doi.org/10.1016/j.jplph.2016.01.002
Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354. https://doi.org/10.1093/jxb/erj014
Varoquaux N, Cole B, Gao C, Pierroz G, Baker CR, Patel D, Madera M, Jeffers T, Hollingsworth J, Sievert J, Yoshinaga Y, Owiti JA, Singan VR, DeGraaf S, Xu L, Blow MJ, Harrison MJ, Visel A, Jansson C et al (2019) Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses. PNAS 116:27124–27132 www.pnas.org/cgi/doi/10.1073/pnas.1907500116
Zelitch I, Waggoner PE (1962) Effect of chemical control of stomata on transpiration and photosynthesis. Proc Natl Acad Sci 48:1101. https://doi.org/10.1073/pnas.48.7.1101
Zhao J, Xue QW, Jessup KE, Hou XB, Hao BZ, Marek TH, Xu WW, Evett SR, Shaughnessy SAO, Brauer DK (2018) Shoot and root traits in drought tolerant maize (Zea mays L.) hybrids. J Integr Agric 17:1093–1105. https://doi.org/10.1016/S2095-3119(17)61869-0
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CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico (National Counsel of Technological and Scientific Development)), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Coordination for the Improvement of Higher Education Personnel)), and FAPEMIG (Fundação de Amparo à Pesquisa do estado de Minas Gerais (Minas Gerais State Research Foundation)) provided funding and research grants awarded to perform the present study.
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J.P.V.O.: conceptualizing, designing and performing the experiments, analyzing the data, curating the data, and writing the first draft of the manuscript; V.P.D.: performing the experiments, analyzing the data, and writing the manuscript; E.M.C.: acquiring resources, analyzing the data, and writing the manuscript; P.C.M. acquiring resources, analyzing the data, and writing the manuscript; F.J.P. advising the first author, conceptualizing, acquiring resources, designing and running the experiments, analyzing the data, curating the data, administering the project, and writing the manuscript.
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de Oliveira, J.P.V., Duarte, V.P., de Castro, E.M. et al. Stomatal cavity modulates the gas exchange of Sorghum bicolor (L.) Moench. grown under different water levels. Protoplasma 259, 1081–1097 (2022). https://doi.org/10.1007/s00709-021-01722-1
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DOI: https://doi.org/10.1007/s00709-021-01722-1