Abstract
Plant’s stomatal physiology and anatomical features are highly plastic and are influenced by diverse environmental signals including the concentration of atmospheric CO2 and nutrient availability. Recent reports suggest that the form of nitrogen (N) is a determinant of plant growth and nutrient nitrogen use efficiency (NUE) under elevated CO2 (EC). Previously, we found that high nitrate availability resulted in early senescence, enhanced reactive oxygen species (ROS), and reactive nitrogen species (RNS) production and also that mixed nutrition of nitrate and ammonium ions were beneficial than sole nitrate nutrition in wheat. In this study, the interactive effects of different N forms (nitrate, ammonium, mixed nutrition of nitrate, and ammonium) and EC on epidermal and stomatal morphology were analyzed. Wheat seedlings were grown at two different CO2 levels and supplied with media devoid of N (N0) or with nitrate–N (NN), mixed nutrition of ammonium and nitrate (MN), or only ammonium-N (AN). The stoma length increased significantly in nitrate nutrition with a consistent reduction in stoma width. Guard cell length was higher in EC treatment as compared to AC. The guard cell width was maximum in AN-grown plants at EC. Epidermal cell density and stomatal density were lower at EC. Nitrate nutrition increased the stomatal area at EC while the reverse was true for MN and AN. Wheat plants fertilized with AN showed a higher accumulation of superoxide radical (SOR) at EC, while in NN treatment, the accumulation of hydrogen peroxide (H2O2) was higher at EC. Reactive oxygen species, particularly H2O2, can trigger mitogen-activated protein kinase (MAPK) mediated signaling and its crosstalk with abscisic acid (ABA) signaling to regulate stomatal anatomy in nitrate-fed plants. The SOR accumulation in ammonium- and ammonium nitrate–fed plants and H2O2 in NN-fed plants might finely regulate the sensitivity of stomata to alter water/nutrient use efficiency and productivity under EC. The data reveals that the variation in anatomical attributes viz. cell length, number of cells, etc. affected the leaf growth responses to EC and forms of N nutrition. These attributes are fine targets for effective manipulation of growth responses to EC.
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References
Adamipour N, Khosh-Khui M, Salehi H et al (2020) Regulation of stomatal aperture in response to drought stress mediating with polyamines, nitric oxide synthase and hydrogen peroxide in Rosa canina L. Plant Signal Behav. https://doi.org/10.1080/15592324.2020.1790844
Adavi SB, Sathee L (2019) Elevated CO2-induced production of nitric oxide differentially modulates nitrate assimilation and root growth of wheat seedlings in a nitrate dose-dependent manner. Protoplasma 256:147–159. https://doi.org/10.1007/s00709-018-1285-2
Adavi SB, Sathee L (2020) Elevated CO2 alters tissue balance of nitrogen metabolism and downregulates nitrogen assimilation and signalling gene expression in wheat seedlings receiving high nitrate supply. Protoplasma 1–15. https://doi.org/10.1007/s00709-020-01564-3
Adavi SB, Sathee L (2021) Elevated CO2 differentially regulates root nitrate transporter kinetics in a genotype and nitrate dose-dependent manner. Plant Sci 305:110807. https://doi.org/10.1016/j.plantsci.2020.110807
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372
Andrews M, Raven JA, Lea PJ (2013) Do plants need nitrate? the mechanisms by which nitrogen form affects plants. Ann Appl Biol 163:174–199
Asif M, Zora S, Ceylan Y et al (2020) Nitrogen supply in combination of nitrate and ammonium enhances harnessing of elevated atmospheric CO2 through improved nitrogen and carbon metabolism in wheat (Triticum aestivum). Crop Pasture Sci 71:101. https://doi.org/10.1071/CP19308
Bahrun A, Jensen CR, Asch F, Mogensen VO (2002) Drought-induced changes in xylem pH, ionic composition, and ABA concentration act as early signals in field-grown maize (Zea mays L.). J Exp Bot 53:251–263. https://doi.org/10.1093/jexbot/53.367.251
Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328(80):899–903
Bright J, Desikan R, Hancock JT et al (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122. https://doi.org/10.1111/j.1365-313X.2005.02615.x
Chater CCC, Oliver J, Casson S, Gray JE (2014) Putting the brakes on: Abscisic acid as a central environmental regulator of stomatal development. New Phytol 202:376–391
Coupe SA, Palmer BG, Lake JA et al (2006) Systemic signalling of environmental cues in Arabidopsis leaves. In: Journal of Experimental Botany, pp 329–341
Cramer MD, Lewis OAM (1993) The influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum) and maize (Zea mays) plants. Ann Bot 72:359–365. https://doi.org/10.1006/anbo.1993.1119
Delucia EH, Sasek TW, Strain BR (1985) Photosynthetic inhibition after long-term exposure to elevated levels of atmospheric carbon dioxide. Photosynth Res 7:175–184. https://doi.org/10.1007/BF00037008
Ding W, Wang Y, Fang W et al (2016) TaZAT8, a C2H2-ZFP type transcription factor gene in wheat, plays critical roles in mediating tolerance to Pi deprivation through regulating P acquisition, ROS homeostasis and root system establishment. Physiol Plant 158:297–311. https://doi.org/10.1111/ppl.12467
Dow GJ, Bergmann DC (2014) Patterning and processes: how stomatal development defines physiological potential. Curr Opin Plant Biol 21:67–74
Driscoll SP, Prins A, Olmos E et al (2006) Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves. In: Journal of Experimental Botany, pp 381–390
Dunn J, Hunt L, Afsharinafar M et al (2019) Reduced stomatal density in bread wheat leads to increased water-use efficiency. J Exp Bot 70:4737–4747. https://doi.org/10.1093/jxb/erz248
Engineer CB, Ghassemian M, Anderson JC et al (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature 513:246–250. https://doi.org/10.1038/nature13452
Estiarte M, Peñuelas J, Kimball BA et al (1994) Elevated CO2 effects on stomatal density of wheat and sour orange trees. J Exp Bot 45:1665–1668. https://doi.org/10.1093/jxb/45.11.1665
Feitosa-Araujo E, da Fonseca-Pereira P, Pena MM et al (2020) Changes in intracellular NAD status affect stomatal development in an abscisic acid-dependent manner. Plant J 104:1149–1168. https://doi.org/10.1111/tpj.15000
Fernández-Crespo E, Scalschi L, Llorens E et al (2015) NH4+ protects tomato plants against Pseudomonas syringae by activation of systemic acquired acclimation. J Exp Bot 66:6777–6790. https://doi.org/10.1093/jxb/erv382
Finkelstein RR, Gibson SI (2002) ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Curr Opin Plant Biol 5:26–32
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609. https://doi.org/10.1105/tpc.12.4.599
Frungillo L, Skelly MJ, Loake GJ et al (2014) S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat Commun 5:5401. https://doi.org/10.1038/ncomms6401
Gray JE, Holroyd GH, van der Lee FM et al (2000) The HIC signalling pathway links CO2 perception to stomatal development. Nature 408:713–716. https://doi.org/10.1038/35047071
Guo F-Q (2003) The Nitrate Transporter AtNRT1.1 (CHL1) Functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. PLANT CELL ONLINE 15:107–117. https://doi.org/10.1105/tpc.006312
Habermann E, Dias de Oliveira EA, Contin DR et al (2019) Stomatal development and conductance of a tropical forage legume are regulated by elevated [CO2] under moderate warming. Front Plant Sci 10:609. https://doi.org/10.3389/fpls.2019.00609
Hachiya T, Sakakibara H (2017) Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and signaling in plants. J Exp Bot 68:2501–2512. https://doi.org/10.1093/JXB/ERW449
He J, Zhang RX, Peng K et al (2018) The BIG protein distinguishes the process of CO2-induced stomatal closure from the inhibition of stomatal opening by CO2. New Phytol 218:232–241. https://doi.org/10.1111/nph.14957
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
Hirel B, Tétu T, Lea PJ, Dubois F (2011) Improving nitrogen use efficiency in crops for sustainable agriculture. Sustainability 3:1452–1485. https://doi.org/10.3390/su3091452
Jauregui I, Aparicio-Tejo PM, Avila C et al (2016) Root-shoot interactions explain the reduction of leaf mineral content in Arabidopsis plants grown under elevated [CO2] conditions. Physiol Plant 158:65–79. https://doi.org/10.1111/ppl.12417
Jauregui I, Aroca R, Garnica M et al (2015) Nitrogen assimilation and transpiration: key processes conditioning responsiveness of wheat to elevated [CO2] and temperature. Physiol Plant 155:338–354. https://doi.org/10.1111/ppl.12345
Kanaoka MM, Pillitteri LJ, Fujii H et al (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20:1775–1785. https://doi.org/10.1105/tpc.108.060848
Lampard GR, MacAlister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322(80):1113–1116. https://doi.org/10.1126/science.1162263
Lee LR, Bergmann DC (2019) The plant stomatal lineage at a glance. J. Cell Sci. 132
Lekshmy S, Jain V, Khetarpal S et al (2016) Influence of elevated carbon dioxide and ammonium nutrition on growth and nitrogen metabolism in wheat (Triticum aestivum). Indian J Agric Sci 86
Lekshmy S, Vanita J, Sangeeta K et al (2009) Effect of elevated carbon dioxide on kinetics of nitrate uptake in wheat roots. Indian J Plant Physiol 14:16–22
León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116
Li D, Li L, Xiao G et al (2018) Effects of elevated CO2 on energy metabolism and γ-aminobutyric acid shunt pathway in postharvest strawberry fruit. Food Chem 265:281–289. https://doi.org/10.1016/j.foodchem.2018.05.106
Li H, Yang Y, Wang H et al (2021) The receptor-like kinase ERECTA confers improved water use efficiency and drought tolerance to poplar via modulating stomatal density. Int J Mol Sci 22:7245. https://doi.org/10.3390/IJMS22147245
Liu Y, von Wirén N (2017) Ammonium as a signal for physiological and morphological responses in plants. J Exp Bot 68:2581–2592. https://doi.org/10.1093/JXB/ERX086
Lopes MS, Araus JL (2006) Nitrogen source and water regime effects on durum wheat photosynthesis and stable carbon and nitrogen isotope composition. Physiol Plant 126:435–445. https://doi.org/10.1111/j.1399-3054.2006.00595.x
Mcallister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: The current status. Plant Biotechnol J 10:1011–1025
Noctor G, Foyer CH (2016) Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol 171:1581–1592. https://doi.org/10.1104/pp.16.00346
Ohashi-Ito K, Bergmann DC (2006) Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18:2493–2505. https://doi.org/10.1105/tpc.106.046136
Padhan BK, Sathee L, Meena HS et al (2020) CO2 Elevation accelerates phenology and alters carbon/nitrogen metabolism vis-à-vis ROS abundance in bread wheat. Front Plant Sci 11:1–18. https://doi.org/10.3389/fpls.2020.01061
Peuke AD, Jeschke WD, Hartung W (1998) Foliar application of nitrate or ammonium as sole nitrogen supply in Ricinus communis. II. The flows of cations, chloride and abscisic acid. New Phytol 140:625–636. https://doi.org/10.1046/j.1469-8137.1998.00304.x
Pillitteri LJ, Bogenschutz NL, Torii KU (2008) The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in arabidopsis. Plant Cell Physiol 49:934–943. https://doi.org/10.1093/pcp/pcn067
Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annu Rev Plant Biol 63:591–614
Quarrie SA, Jones HG (1977) Effects of abscisic acid and water stress on development and morphology of wheat. J Exp Bot 28:192–203. https://doi.org/10.1093/jxb/28.1.192
Rasmusson AG, Escobar MA, Hao M et al (2020) Mitochondrial NAD(P)H oxidation pathways and nitrate/ammonium redox balancing in plants. Mitochondrion 53:158–165
Robertson EJ, Leech RM (1995) Significant changes in cell and chloroplast development in young wheat leaves (Triticum aestivum cv Hereward) grown in elevated CO2. Plant Physiol 107:63–71. https://doi.org/10.1104/pp.107.1.63
Robredo A, Pérez-López U, de la Maza HS et al (2007) Elevated CO2 alleviates the impact of drought on barley improving water status by lowering stomatal conductance and delaying its effects on photosynthesis. Environ Exp Bot 59:252–263. https://doi.org/10.1016/j.envexpbot.2006.01.001
Rubio-Asensio JS, Bloom AJ (2017) Inorganic nitrogen form: a major player in wheat and Arabidopsis responses to elevated CO 2. J Exp Bot. https://doi.org/10.1093/jxb/erw465
Sathee L, Adavi SB, Jain V et al (2018) Influence of Elevated CO2 on kinetics and expression of high affinity nitrate transport systems in wheat. Indian J Plant Physiol 23:111–117. https://doi.org/10.1007/s40502-018-0355-y
Sathee L, Meena HS, Adavi SB, Jha SK (2019) Cross talk of nitric oxide and reactive oxygen species in various processes of plant development: past and present. Plant Abiotic Stress Tolerance. Springer International Publishing, Cham, pp 381–408
See D, Kanazin V, Kephart K, Blake T (2002) Mapping genes controlling variation in barley grain protein concentration. Crop Sci 42:680–685. https://doi.org/10.2135/cropsci2002.6800
Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621
Tcherkez G, Ben Mariem S, Larraya L et al (2020) Elevated CO2 has concurrent effects on leaf and grain metabolism but minimal effects on yield in wheat. J Exp Bot 71:5990–6003. https://doi.org/10.1093/jxb/eraa330
Tichá I (1982) Photosynthetic characteristics during ontogenesis of leaves. 7 Stomatal density and sizes. Photosynthetica 16:375–471
Torralbo F, González-Moro MB, Baroja-Fernández E et al (2019) Differential regulation of stomatal conductance as a strategy to cope with ammonium fertilizer under ambient versus elevated CO2. Front Plant Sci 10:597. https://doi.org/10.3389/fpls.2019.00597
Uprety DC, Dwivedi N, Jain V, Mohan R (2002) Effect of elevated carbon dioxide concentration on the stomatal parameters of rice cultivars. Photosynthetica 40:315–319. https://doi.org/10.1023/A:1021322513770
Van Oosten J-J, Besford RT (1996) Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: climate of opinion. Photosynth Res 48:353–365. https://doi.org/10.1007/BF00029468
Vatén A, Soyars CL, Tarr PT et al (2018) Modulation of asymmetric division diversity through cytokinin and SPEECHLESS regulatory interactions in the Arabidopsis stomatal lineage. Dev Cell 47:53-66.e5. https://doi.org/10.1016/j.devcel.2018.08.007
Wang X, Wei X, Wu G, Chen S (2020) High nitrate or ammonium applications alleviated photosynthetic decline of phoebe bournei seedlings under elevated carbon dioxide. Forests 11:293. https://doi.org/10.3390/f11030293
Watling JR, Press MC, Quick WP (2000) Elevated CO2 induces biochemical and ultrastructural changes in leaves of the C4 cereal sorghum. Plant Physiol 123:1143–1152. https://doi.org/10.1104/pp.123.3.1143
Webb AAR, Hetherington AM (1997) Convergence of the abscisic acid, CO2, and extracellular calcium signal transduction pathways in stomatal guard cells. Plant Physiol 114:1557–1560. https://doi.org/10.1104/pp.114.4.1557
Winter K, Usuda H, Tsuzuki M et al (1982) Influence of nitrate and ammonia on photosynthetic characteristics and leaf anatomy of Moricandia arvensis. Plant Physiol 70:616–625. https://doi.org/10.1104/pp.70.2.616
Wolf DD, Carson EW, Parrish DJ (1979) A replica method of determining stomatal and epidermal cell density. J Agron Educ 8:52–54. https://doi.org/10.2134/jae.1979.0052
Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618
Woodward FI, Bazzaz FA (1988) The responses of stomatal density to CO2 partial pressure. J Exp Bot 39:1771–1781. https://doi.org/10.1093/JXB/39.12.1771
Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytol 131:311–327. https://doi.org/10.1111/j.1469-8137.1995.tb03067.x
Zheng Y, Li F, Hao L et al (2019) Elevated CO2 concentration induces photosynthetic down-regulation with changes in leaf structure, non-structural carbohydrates and nitrogen content of soybean. BMC Plant Biol 19. https://doi.org/10.1186/s12870-019-1788-9
Acknowledgements
The authors are thankful to the ICAR-Indian Agricultural Research Institute for funding and providing the necessary facilities. LS acknowledges ICAR- Junior research fellowship support received during the study. The authors acknowledge the technical help received from Dr. Sangeeta Khetarpal (plant culture) and Mr. Hari S Meena (ROS localization). The authors also acknowledge suggestions from Dr. Renu Pandey and Dr. SK Jha while finalizing the experiment and the final draft respectively.
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LS conducted the experiments, analyzed the data, and finalized the manuscript. VJ and LS finalized the experiments. VJ provided reagents and materials required for the study.
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Sathee, L., Jain, V. Interaction of elevated CO2 and form of nitrogen nutrition alters leaf abaxial and adaxial epidermal and stomatal anatomy of wheat seedlings. Protoplasma 259, 703–716 (2022). https://doi.org/10.1007/s00709-021-01692-4
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DOI: https://doi.org/10.1007/s00709-021-01692-4