Abstract
The objectives of this study were to investigate stomatal regulation in maize seedlings during progressive soil drying and to determine the impact of stomatal movement on photosynthetic activity. In well-watered and drought-stressed plants, leaf water potential (Ψ leaf), relative water content (RWC), stomatal conductance (g s), photosynthesis, chlorophyll fluorescence, leaf instantaneous water use efficiency (iWUEleaf), and abscisic acid (ABA) and zeatin-riboside (ZR) accumulation were measured. Results showed that g s decreased significantly with progressive drought and stomatal limitations were responsible for inhibiting photosynthesis in the initial stages of short-term drought. However, after 5 days of withholding water, non-stomatal limitations, such as damage to the PSII reaction center, became the main limiting factor. Stomatal behavior was correlated with changes in both hydraulic and chemical signals; however, changes in ABA and ZR occurred prior to any change in leaf water status. ABA in leaf and root tissue increased progressively during soil drying, and further analysis found that leaf ABA was negatively correlated with g s (R 2 = 0.907, p < 0.05). In contrast, leaf and root ZR decreased gradually. ZR in leaf tissue was positively correlated with g s (R 2 = 0.859, p < 0.05). These results indicate that ABA could induce stomatal closure, and ZR works antagonistically against ABA in stomatal behavior. In addition, the ABA/ZR ratio also had a strong correlation with g s, suggesting that the combined chemical signal (the interaction between ABA and cytokinin) plays a role in coordinating stomatal behavior. In addition, Ψ leaf and RWC decreased significantly after only 3 days of drought stress, also affecting stomatal behavior.
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Abbreviations
- ABA:
-
Abscisic acid
- C a :
-
Ambient CO2 concentration
- C i :
-
Intercellular CO2 concentration
- C i/C a :
-
Ratio of intercellular to ambient CO2 concentration
- CK:
-
Cytokinin
- E :
-
Transpiration rate
- F o :
-
Minimum fluorescence yield
- \(F_{\text{o}}^{'}\) :
-
Minimum fluorescence in the light
- F m :
-
The maximum fluorescence yield
- \(F_{\text{m}}^{'}\) :
-
The maximum fluorescence in the light
- F s :
-
The steady-state fluorescence yield
- F v /F m :
-
The maximum efficiency of PSII
- g s :
-
Stomatal conductance
- L s :
-
Stomatal limitation value
- NPQ:
-
Non-photochemical quenching
- P n :
-
Photosynthetic rate
- qP:
-
Photochemical quenching
- RWC:
-
Relative water content
- iWUEleaf :
-
Leaf instantaneous water use efficiency
- ZR:
-
Zeatin-riboside
- Ψ leaf :
-
Leaf water potential
- Φ PSII :
-
Actual efficiency of PSII
References
Allen RG (2000) Using the FAO-56 dual crop coefficient method over an irrigated region as part of an evapotranspiration intercomparison study. J Hydrol 229:27–41
Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56:1535–1544
Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM (2011) Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J Agron Crop Sci 197:177–185
Atkinson CJ, Policarpo M, Webster AD, Kingswell G (2000) Drought tolerance of clonal Malus determined from measurements of stomatal conductance and leaf water potential. Tree Physiol 20:557–563
Berkowitz GA, Chen C, Gibbs M (1983) Stromal acidification mediates in vivo water stress inhibition of nonstomatal-controlled photosynthesis. Plant Physiol 72:1123–1126
Berry JA, Downton WJS (1982) Environmental regulation of photosynthesis. Photosynthesis 2:263–343
Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
Chen SL, Wang SS, Arie A, Aloys H (1996) Cytokinins: moderators of stomatal movement in poplar genotypes. J Beijing For Univ (Einglish Ed.) 5:9–22
Chen YN, Wang Q, Ruan X, Li WH, Chen YP (2004) Physiological response of Populus euphratica to artificial water-recharge of the lower reaches of Tarim River. Acta Bot Sin 46:1393–1401
Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174
Cornic G, Briantais JM (1991) Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183:178–184
Davies WJ, Hartung W (2004) Has extrapolation from biochemistry to crop functioning worked to sustain plant production under water scarcity? In: Proceedings of the 4th international crop science congress, Brisbane, Australia, pp 1–14
Davies WJ, Kudoyarova G, Hartung W (2005) Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. J Plant Growth Regul 24:285–295
Dodd IC, Puértolas J, Huber K, Pérez-Pérez JG, Wright HR, Blackwell MSA (2015) The importance of soil drying and re-wetting in crop phytohormonal and nutritional responses to deficit irrigation. J Exp Bot 66:2239–2252
Dörffling K, Streich J, Kruse W, Muxfeldt B (1977) Abscisic acid and the after-effect of water stress on stomatal opening potential. Z Pflanzenphysiol 81:43–56
Edmeades GO, Chapman SC, Lafitte HR (1999) Selection improves drought tolerance in tropical maize populations: I. Gains in biomass, grain yield, and harvest index. Crop Sci 39:1306–1315
Else MA, Coupland D, Dutton L, Jackson MB (2001) Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiol Plant 111:46–54
Escalona JM, Flexas J, Medrano H (1999) Stomatal and non-stomatal limitations of photosynthesis under water stress in field-grown grapevines. Aust J Plant Physiol 26:421–433
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345
Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot Lond 89:183–189
Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050
Gong H, Chen K (2012) The regulatory role of silicon on water relations, photosynthetic gas exchange, and carboxylation activities of wheat leaves in field drought conditions. Acta Physiol Plant 34:1589–1594
Grzesiak MT, Rzepka A, Hura T, Grzesiak S, Hura K, Filek W, Skoczowski A (2007) Fluorescence excitation spectra of drought resistant and sensitive genotypes of triticale and maize. Photosynthetica 45:606–611
Grzesiak MT, Hura T, Grzesiak S, Pilarski J (2009) Effect of drought stress on leaf optical properties in drought-resistant and drought-sensitive maize and triticale genotypes. Photosynthetica 47:635–637
Hansen H, Dörffling K (1999) Changes of free and conjugated abscisic acid and phaseic acid in xylem sap of drought-stressed sunflower plants. J Exp Bot 50:1599–1605
He Z (1993) A laboratory guide to chemical control technology on field crop. Beijing Agricultural University Press, Beijing
Holbrook NM, Shashidhar VR, James RA, Munns R (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J Exp Bot 53:1503–1514
Hsiao TC, Xu LK (1999) Predicting water use efficiency of crops. In: Ferreira MI, Jones HG (eds) International symposium on irrigation of horticultural crops, 3rd edn, pp 199–206
Huang Z, Zou Z, He C, He Z, Zhang Z, Li J (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339:391–399
Hura T, Hura K, Grzesiak M, Rzepka A (2007) Effect of long-term drought stress on leaf gas exchange and fluorescence parameters in C3 and C4 plants. Acta Physiol Plant 29:103–113
Jacobsen SE, Liu F, Jensen CR (2009) Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). Sci Hortic Amst 122:281–287
Janowiak F, Dörffling K (1996) Chilling of maize seedlings: changes in water status and abscisic acid content in ten genotypes differing in chilling tolerance. J Plant Physiol 147:582–588
Janowiak F, Maas B, Dörffling K (2002) Importance of abscisic acid for chilling tolerance of maize seedlings. J Plant Physiol 159:635–643
Jokhan AD, Else MA, Jackson MB (1996) Delivery rates of abscisic acid in xylem sap of Ricinus communis L. plants subjected to part-drying of the soil. J Exp Bot 47:1595–1599
Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685
Kang S, Zhang J (2004) Controlled alternate partial root-zone irrigation: its physiological consequences and impact on water use efficiency. J Exp Bot 55:2437–2446
Kang S, Shi W, Zhang J (2000) An improved water-use efficiency for maize grown under regulated deficit irrigation. Field Crop Res 67:207–214
Koprowski M, Robertson I, Wils THG, Kalaji HM (2015) The application of potato starch effluent causes a reduction in the photosynthetic efficiency and growth of Scots pine (Pinus sylvestris L.). Trees 29:1471–1481
Lal A, Ku MSB, Edwards GE (1996) Analysis of inhibition of photosynthesis due to water stress in the C3 species Hordeum vulgare and Vicia faba: electron transport, CO2 fixation and carboxylation capacity. Photosynth Res 49:57–69
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570
Li X, Xu K (2014) Effects of exogenous hormones on leaf photosynthesis of Panax ginseng. Photosynthetica 52:152–156
Liang J, Zhang J, Wong MH (1997) Can stomatal closure caused by xylem ABA explain the inhibition of leaf photosynthesis under soil drying? Photosynth Res 51:149–159
Liu F, Andersen MN, Jacobsen SE, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environ Exp Bot 54:33–40
Liu F, Shahnazari A, Andersen MN, Jacobsen SE, Jensen CR (2006) Physiological responses of potato (Solanum tuberosum L.) to partial root-zone drying: ABA signalling, leaf gas exchange, and water use efficiency. J Exp Bot 57:3727–3735
Malone M (1993) Hydraulic signals. Philos Trans R Soc B 341:33–39
Nilson SE, Assmann SM (2007) The control of transpiration. Insights from Arabidopsis. Plant Physiol 143:19–27
Pantin F, Monnet F, Jannaud D, Costa JM, Renaud J, Muller B, Simonneau T, Genty B (2013) The dual effect of abscisic acid on stomata. New Phytol 197:65–72
Pospíšilová J, Synková H, Rulcová J (2000) Cytokinins and water stress. Biol Plant 43:321–328
Qiu N, Lu Q, Lu C (2003) Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex centralasiatica. New Phytol 159:479–486
Raeini-Sarjaz M, Barthakur NN, Arnold NP, Jones PJH (1998) Water stress, water use efficiency, carbon isotope discrimination and leaf gas exchange relationships of the bush bean. J Agron Crop Sci 180:173–179
Schachtman DP, Goodger JQD (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13:281–287
Shangguan Z, Shao M, Dyckmans J (1999) Interaction of osmotic adjustment and photosynthesis in winter wheat under soil drought. J Plant Physiol 154:753–758
Sobeih WY, Dodd IC, Bacon MA, Grierson D, Davies WJ (2004) Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying. J Exp Bot 55:2353–2363
Souza RP, Machado EC, Silva JAB, Lagôa AMMA, Silveira JAG (2004) Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ Exp Bot 51:45–56
Stikic R, Popovic S, Srdic M, Savic D, Jovanovic Z, Prokic LJ, Zdravkovic J (2003) Partial root drying (PRD): a new technique for growing plants that saves water and improves the quality of fruit. Bulg J Plant Physiol 29:164–171
Stoll M, Loveys B, Dry P (2000) Hormonal changes induced by partial rootzone drying of irrigated grapevine. J Exp Bot 51:1627–1634
Tardieu F, Davies WJ (1992) Stomatal response to abscisic acid is a function of current plant water status. Plant Physiol 98:540–545
Weatherley PE (1950) Studies in the water relations of the cotton plant. New Phytol 49:81–97
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210
Wójcik-Jagła M, Rapacz M, Barcik W, Janowiak F (2012) Differential regulation of barley (Hordeum distichon) HVA1 and SRG6 transcript accumulation during the induction of soil and leaf water deficit. Acta Physiol Plant 34:2069–2078
Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325
Zlatev ZS, Yordanov IT (2004) Effects of soil drought on photosynthesis and chlorophyll fluorescence in bean plants. Bulg J Plant Physiol 30:3–18
Żur I, Dubas E, Krzewska M, Waligórski P, Dziurka M, Janowiak F (2015) Hormonal requirements for effective induction of microspore embryogenesis in triticale (× Triticosecale Wittm.) anther cultures. Plant Cell Rep 34:47–62
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This study was financially supported by National Natural Science Foundation of China (51409131) and Jiangxi Province Science and Technology Support Program, China (20151BBF60013).
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Communicated by P. Sowinski.
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Yan, H., Wu, L., Filardo, F. et al. Chemical and hydraulic signals regulate stomatal behavior and photosynthetic activity in maize during progressive drought. Acta Physiol Plant 39, 125 (2017). https://doi.org/10.1007/s11738-017-2418-5
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DOI: https://doi.org/10.1007/s11738-017-2418-5