Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Similar soil drying-induced stomatal closure in soybean genotypes varying in abscisic acid accumulation and stomatal sensitivity to abscisic acid

Pedro Castro-Valdecantos https://orcid.org/0000-0002-8543-9391 A B C D * , Jaime Puértolas A E and Ian C. Dodd A C
+ Author Affiliations
- Author Affiliations

A Lancaster Environment Centre, Lancaster LA1 4YQ, UK.

B School of Life Sciences and Centre for Soybean Research of the State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Sha Tin, Hong Kong, China.

C The Joint Institute for the Environmental Research and Education, Guangzhou, China.

D Present address: Department of Agronomy, Escuela Técnica Superior de Ingeniería Agronómica, University of Seville, Ctra. Utrera km. 1, Seville 41013, Spain.

E Present address: Department of Botany and Plant Ecology and Physiology, University of La Laguna, Facultad de Farmacia, Avd Astrofísico Francisco Sánchez s/n, San Cristóbal de La Laguna, Canary Islands 38200, Spain.

* Correspondence to: pcvaldecantos@us.es

Handling Editor: Muhammad Waseem

Functional Plant Biology 51, FP23012 https://doi.org/10.1071/FP23012
Submitted: 10 January 2023  Accepted: 21 March 2023  Published: 19 April 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Different soybean cultivars (Williams 82, Union, Jindou 21, Long Huang 1, Long Huang 2) were exposed to drying soil, to investigate whether endogenous abscisic acid (ABA) concentrations and leaf water relations regulated stomatal behaviour. We measured ABA concentrations in xylem and tissue of the first and second trifoliate leaves respectively; stomatal conductance (gs) and leaf water potential (Ψleaf) in both leaves; and water content in soil. Cultivar variation in leaf area and gs caused different rates of soil drying, but gs and Ψleaf declined similarly with soil drying in all cultivars. Variation in leaf xylem ABA concentration better explained stomatal responses than foliar ABA concentration in some cultivars, and was highly correlated with stomatal conductance. Xylem ABA concentration in well-watered soil was highest in Union, and in drying soil was lowest in Jindou 21 and Long Huang 2, although the latter had the highest foliar ABA concentrations. Jindou 21 accumulated lower xylem ABA concentrations than other cultivars as soil moisture or Ψleaf decreased, but its stomatal sensitivity to xylem ABA was greater. Because cultivars varied in both ABA accumulation and stomatal sensitivity to ABA, but had similar stomatal sensitivity to Ψleaf, leaf water relations seem more important in regulating stomatal closure of soybean.

Keywords: ABA, drought, genotypic variation, Glycine max, physiological responses, stomatal closure, water status, water stress.

References

Bennett JM, Sinclair TR, Muchow RC, Costello SR (1987) Dependence of stomatal conductance on leaf water potential, turgor potential, and relative water content in field-grown soybean and maize 1. Crop Science 27(5), 984-990.
| Crossref | Google Scholar |

Bernard RL, Lindahl DA (1972) Registration of Williams Soybean1 (Reg. No. 94). Crop Science 12(5), 716.
| Crossref | Google Scholar |

Blum A, Sinmena B (1995) Isolation and characterization of variant wheat cultivars for ABA sensitivity. Plant, Cell and Environment 18(1), 77-83.
| Crossref | Google Scholar |

Borel C, Simonneau T (2002) Is the ABA concentration in the sap collected by pressurizing leaves relevant for analysing drought effects on stomata? Evidence from ABA-fed leaves of transgenic plants with modified capacities to synthesize ABA. Journal of Experimental Botany 53(367), 287-296.
| Crossref | Google Scholar |

Bruce WB, Edmeades GO, Barker TC (2002) Molecular and physiological approaches to maize improvement for drought tolerance. Journal of Experimental Botany 53(366), 13-25.
| Crossref | Google Scholar |

Bunce JA (1977) Leaf elongation in relation to leaf water potential in soybean. Journal of Experimental Botany 28, 156-161.
| Crossref | Google Scholar |

Castro P, Puertolas J, Dodd IC (2019) Stem girdling uncouples soybean stomatal conductance from leaf water potential by enhancing leaf xylem ABA concentration. Environmental and Experimental Botany 159, 149-156.
| Crossref | Google Scholar |

Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 42, 55-76.
| Crossref | Google Scholar |

Dodd IC (2005) Root-to-shoot signalling: assessing the roles of ‘up’ in the up and down world of long-distance signalling in planta. Plant and Soil 274(1), 251-270.
| Crossref | Google Scholar |

Dodd IC (2007) Soil moisture heterogeneity during deficit irrigation alters root-to-shoot signalling of abscisic acid. Functional Plant Biology 34(5), 439.
| Crossref | Google Scholar |

Feng Y-Y, Richards RA, Jin Y, Siddique KHM, Li F-M, He J (2022) Yield and water-use related traits in landrace and new soybean cultivars in arid and semi-arid areas of China. Field Crops Research 283, 108559.
| Crossref | Google Scholar |

Fried HG, Narayanan S, Fallen B (2019) Evaluation of soybean [Glycine max (L.) Merr.] genotypes for yield, water use efficiency, and root traits. PLoS ONE 14(2), e0212700.
| Crossref | Google Scholar |

Gebre MG, Rajcan I, Earl HJ (2022) Genetic variation for effects of drought stress on yield formation traits among commercial soybean [Glycine max (L.) Merr.] cultivars adapted to Ontario, Canada. Frontiers in Plant Science 13, 1020944.
| Crossref | Google Scholar |

Gilbert ME, Zwieniecki MA, Holbrook NM (2011) Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. Journal of Experimental Botany 62(8), 2875-2887.
| Crossref | Google Scholar |

Ha CV, Watanabe Y, Tran UT, Le DT, Tanaka M, Nguyen KH, Seki M, Nguyen DV, Tran L-SP (2015) Comparative analysis of root transcriptomes from two contrasting drought-responsive Williams 82 and DT2008 soybean cultivars under normal and dehydration conditions. Frontiers in Plant Science 6, 551.
| Crossref | Google Scholar |

He J, Du Y-L, Wang T, Turner NC, Xi Y, Li F-M (2016) Old and new cultivars of soya bean (Glycine max L.) subjected to soil drying differ in abscisic acid accumulation, water relations characteristics and yield. Journal of Agronomy and Crop Science 202(5), 372-383.
| Crossref | Google Scholar |

Hossain MM, Liu X, Qi X, Lam H-M, Zhang J (2014) Differences between soybean genotypes in physiological response to sequential soil drying and rewetting. The Crop Journal 2(6), 366-380.
| Crossref | Google Scholar |

Hossain MM, Lam H-M, Zhang J (2015) Responses in gas exchange and water status between drought-tolerant and -susceptible soybean genotypes with ABA application. The Crop Journal 3(6), 500-506.
| Crossref | Google Scholar |

Hufstetler EV, Boerma HR, Carter TE, Earl HJ (2007) Genotypic variation for three physiological traits affecting drought tolerance in soybean. Crop Science 47(1), 25-35.
| Crossref | Google Scholar |

Ismail MR, Davies WJ, Awad MH (2002) Leaf growth and stomatal sensitivity to ABA in droughted pepper plants. Scientia Horticulturae 96(1-4), 313-327.
| Crossref | Google Scholar |

Jin Y, He J, Turner NC, Du Y-L, Li F-M (2019) Water-conserving and biomass-allocation traits are associated with higher yields in modern cultivars compared to landraces of soybean [Glycine max (L.) Merr.] in rainfed water-limited environments. Environmental and Experimental Botany 168, 103883.
| Crossref | Google Scholar |

King CA, Purcell LC, Brye KR (2009) Differential wilting among soybean genotypes in response to water deficit. Crop Science 49(1), 290-298.
| Crossref | Google Scholar |

Ku Y-S, Ni M, Muñoz NB, Xiao Z, Lo AW-Y, Chen P, Li M-W, Cheung M-Y, Xie M, Lam H-M (2020) ABAS1 from soybean is a 1R-subtype MYB transcriptional repressor that enhances ABA sensitivity. Journal of Experimental Botany 71(10), 2970-2981.
| Crossref | Google Scholar |

Kulkarni MJ, Prasad TG, Sashidhar VR (2000) Genotypic variation in ‘early warning signals’ from roots in drying soil: intrinsic differences in ABA synthesising capacity rather than root density determines total ABA ‘message’ in cowpea (Vigna unguiculata L.). Annals of Applied Biology 136(3), 267-272.
| Crossref | Google Scholar |

Lam H-M, Xu X, Liu X, Chen W, Yang G, Wong F-L, Li M-W, He W, Qin N, Wang B, Li J, Jian M, Wang J, Shao G, Wang J, Sun SS-M, Zhang G (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nature Genetics 42(12), 1053-1059.
| Crossref | Google Scholar |

Li W, de Ollas C, Dodd IC (2018) Long-distance ABA transport can mediate distal tissue responses by affecting local ABA concentrations. Journal of Integrative Plant Biology 60(1), 16-33.
| Crossref | Google Scholar |

Li S, Li X, Wei Z, Liu F (2020) ABA-mediated modulation of elevated CO2 on stomatal response to drought. Current Opinion in Plant Biology 56, 174-180.
| Crossref | Google Scholar |

Liu F, Jensen CR, Andersen MN (2003) Hydraulic and chemical signals in the control of leaf expansion and stomatal conductance in soybean exposed to drought stress. Functional Plant Biology 30, 65-73.
| Crossref | Google Scholar |

Liu F, Andersen MN, Jacobsen S-E, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environmental and Experimental Botany 54, 33-40.
| Crossref | Google Scholar |

Liu H, Song F, Liu S, Liu F, Zhu X (2018) Physiological response of maize and soybean to partial root-zone drying irrigation under N fertilization levels. Emirates Journal of Food and Agriculture 364-371.
| Crossref | Google Scholar |

Manavalan LP, Guttikonda SK, Phan Tran L-S, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant and Cell Physiology 50(7), 1260-1276.
| Crossref | Google Scholar |

Martin-Vertedor AI, Dodd IC (2011) Root-to-shoot signalling when soil moisture is heterogeneous: increasing the proportion of root biomass in drying soil inhibits leaf growth and increases leaf abscisic acid concentration. Plant, Cell and Environment 34(7), 1164-1175.
| Crossref | Google Scholar |

Netting AG, Theobald JC, Dodd IC (2012) Xylem sap collection and extraction methodologies to determine in vivo concentrations of ABA and its bound forms by gas chromatography-mass spectrometry (GC-MS). Plant Methods 8, 11.
| Crossref | Google Scholar |

Passioura JB, Munns R (1984) Hydraulic resistance of plants. II. Effects of rooting medium, and time of day, in barley and lupin. Functional Plant Biology 11(5), 341-350.
| Crossref | Google Scholar |

Pathan SM, Lee J-D, Sleper DA, Fritschi FB, Sharp RE, Carter TE, Jr, Nelson RL, King CA, Schapaugh WT, Ellersieck MR, Nguyen HT, Shannon JG (2014) Two soybean plant introductions display slow leaf wilting and reduced yield loss under drought. Journal of Agronomy and Crop Science 200(3), 231-236.
| Crossref | Google Scholar |

Prince SJ, Vuong TD, Wu X, Bai Y, Lu F, Kumpatla SP, Valliyodan B, Shannon JG, Nguyen HT (2020) Mapping quantitative trait loci for soybean seedling shoot and root architecture traits in an inter-specific genetic population. Frontiers in Plant Science 11, 1284.
| Crossref | Google Scholar |

Puértolas J, Conesa MR, Ballester C, Dodd IC (2015) Local root abscisic acid (ABA) accumulation depends on the spatial distribution of soil moisture in potato: implications for ABA signalling under heterogeneous soil drying. Journal of Experimental Botany 66(8), 2325-2334.
| Crossref | Google Scholar |

Quarrie SA, Whitford PN, Appleford NEJ, Wang TL, Cook SK, Henson IE, Loveys BR (1988) A monoclonal antibody to (S)-abscisic acid: its characterisation and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173(3), 330-339.
| Crossref | Google Scholar |

Saleem A, Roldán-Ruiz I, Aper J, Muylle H (2022) Genetic control of tolerance to drought stress in soybean. BMC Plant Biology 22(1), 615.
| Crossref | Google Scholar |

Saradadevi R, Bramley H, Siddique KHM, Edwards E, Palta JA (2014) Contrasting stomatal regulation and leaf ABA concentrations in wheat genotypes when split root systems were exposed to terminal drought. Field Crops Research 162, 77-86.
| Crossref | Google Scholar |

Sinclair TR, Zwieniecki MA, Holbrook NM (2008) Changes in plant–soil hydraulic pressure gradients of soybean in response to soil drying. Annals of Applied Biology 152(1), 49-57.
| Crossref | Google Scholar |

Sinclair TR, Messina CD, Beatty A, Samples M (2010) Assessment across the United States of the benefits of altered soybean drought traits. Agronomy Journal 102(2), 475-482.
| Crossref | Google Scholar |

Trejo CL, Davies WJ (1991) Drought-Induced closure of Phaseolus vulgaris L. stomata precedes leaf water deficit and any increase in xylem ABA concentration. Journal of Experimental Botany 42(12), 1507-1516.
| Crossref | Google Scholar |

Wang Z, Huang B (2003) Genotypic variation in abscisic acid accumulation, water relations, and gas exchange for Kentucky bluegrass exposed to drought stress. Journal of the American Society for Horticultural Science 128(3), 349-355.
| Crossref | Google Scholar |

Wang Z, Huang C, Niu Y, Yung W-S, Xiao Z, Wong F-L, Huang M, Wang X, Man C-K, Sze C-C, Liu A, Wang Q, Chen Y, Liu S, Wu C, Liu L, Hou W, Han T, Li M-W, Lam H-M (2022) QTL analyses of soybean root system architecture revealed genetic relationships with shoot-related traits. Theoretical and Applied Genetics 135, 4507-4522.
| Crossref | Google Scholar |

Wilkinson S, Corlett JE, Oger L, Davies WJ (1998) Effects of xylem pH on transpiration from wild-type and flacca tomato leaves: a vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiology 117(2), 703-709.
| Crossref | Google Scholar |

Xu C, Xia C, Xia Z, Zhou X, Huang J, Huang Z, Liu Y, Jiang Y, Casteel S, Zhang C (2018) Physiological and transcriptomic responses of reproductive stage soybean to drought stress. Plant Cell Reports 37, 1611-1624.
| Crossref | Google Scholar |

Zhang J, Davies WJ (1990) Changes in the concentration of ABA in xylem sap as a function of changing soil water status can account for changes in leaf conductance and growth. Plant, Cell and Environment 13(3), 277-285.
| Crossref | Google Scholar |