Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

High-throughput phenotyping of soybean (Glycine max) transpiration response curves to rising atmospheric drying in a mapping population

Daniel Monnens A , José R. López A , Erik McCoy A , Bishal G. Tamang A , Aaron J. Lorenz A and Walid Sadok https://orcid.org/0000-0001-9637-2412 A *
+ Author Affiliations
- Author Affiliations

A Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN 55108, USA.

* Correspondence to: msadok@umn.edu

Handling Editor: Kang Yu

Functional Plant Biology 51, FP23281 https://doi.org/10.1071/FP23281
Submitted: 14 November 2023  Accepted: 8 November 2024  Published: 21 November 2024

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

Abstract

In soybean (Glycine max), limiting whole-plant transpiration rate (TR) response to increasing vapor pressure deficit (VPD) has been associated with the ‘slow-wilting’ phenotype and with water-conservation enabling higher yields under terminal drought. Despite the promise of this trait, it is still unknown whether it has a genetic basis in soybean, a challenge limiting the prospects of breeding climate-resilient varieties. Here, we present the results of a first attempt at a high-throughput phenotyping of TR and stomatal conductance response curves to increasing VPD conducted on a soybean mapping population consisting of 140 recombinant inbred lines (RIL). This effort was conducted over two consecutive years, using a controlled-environment, gravimetric phenotyping platform that enabled characterizing 900 plants for these responses, yielding regression parameters (R2 from 0.92 to 0.99) that were used for genetic mapping. Several quantitative trait loci (QTL) were identified for these parameters on chromosomes (Ch) 4, 6, and 10, including a VPD-conditional QTL on Ch 4 and a ‘constitutive’ QTL controlling all parameters on Ch 6. This study demonstrated for the first time that canopy water use in response to rising VPD has a genetic basis in soybean, opening novel avenues for identifying alleles enabling water conservation under current and future climate scenarios.

Keywords: climate change, drought, legumes, soybean, stomata conductance, transpiration, vapor pressure deficit, yield.

References

Bates DM, Watts DG (1988) ‘Nonlinear regression analysis and its applications.’ (John Wiley & Sons: Hoboken, NJ, USA)

Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19(7), 889-890.
| Crossref | Google Scholar | PubMed |

Broman KW, Gatti DM, Simecek P, Furlotte NA, Prins P, Sen Ś, Yandell BS, Churchill GA (2019) R/qtl2: software for mapping quantitative trait loci with high-dimensional data and multiparent populations. Genetics 211(2), 495-502.
| Crossref | Google Scholar | PubMed |

Carpentieri-Pipolo V, Pipolo AE, Abdel-Haleem H, Boerma HR, Sinclair TR (2012) Identification of QTLs associated with limited leaf hydraulic conductance in soybean. Euphytica 186, 679-686.
| Crossref | Google Scholar |

Carter TE, Todd SM, Gillen AM (2016) Registration of ‘USDA-N8002’ soybean cultivar with high yield and abiotic stress resistance traits. Journal of Plant Registrations 10, 238-245.
| Crossref | Google Scholar |

Devi JM, Sinclair TR, Chen P, Carter TE (2014) Evaluation of elite southern maturity soybean breeding lines for drought-tolerant traits. Agronomy Journal 106, 1947-1954.
| Crossref | Google Scholar |

Diers BW, Specht J, Rainey KM, Cregan P, Song Q, Ramasubramanian V, Graef G, Nelson R, Schapaugh W, Wang D, Shannon G, McHale L, Kantartzi SK, Xavier A, Mian R, Stupar RM, Michno JM, Charles An Y-Q, Goettel W, Ward R, Fox C, Lipka AE, Hyten D, Cary T, Beavis WD (2018) Genetic architecture of soybean yield and agronomic traits. G3 Genes|Genomes|Genetics 8(10), 3367-3375.
| Crossref | Google Scholar | PubMed |

Ficklin DL, Novick KA (2017) Historic and projected changes in vapor pressure deficit suggest a continental-scale drying of the United States atmosphere. Journal of Geophysical Research: Atmospheres 122, 2061-2079.
| Crossref | Google Scholar |

Fletcher AL, Sinclair TR, Allen LH, Jr. (2007) Transpiration responses to vapor pressure deficit in well watered ‘slow-wilting’ and commercial soybean. Environmental and Experimental Botany 61(2), 145-151.
| Crossref | Google Scholar |

Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Research 38, D843-D846.
| Crossref | Google Scholar | PubMed |

Grossiord C, Buckley TN, Cernusak LA, Novick KA, Poulter B, Siegwolf RTW, Sperry JS, McDowell NG (2020) Plant responses to rising vapor pressure deficit. New Phytologist 226, 1550-1566.
| Crossref | Google Scholar | PubMed |

Kimm H, Guan K, Gentine P, Wu J, Bernacchi CJ, Sulman BN, Griffis TJ, Lin C (2020) Redefining droughts for the U.S. Corn Belt: the dominant role of atmospheric vapor pressure deficit over soil moisture in regulating stomatal behavior of Maize and Soybean. Agricultural and Forest Meteorology 287, 107930.
| Crossref | Google Scholar |

Kruijer W, Boer MP, Malosetti M, Flood PJ, Engel B, Kooke R, Keurentjes JJB, van Eeuwijk FA (2015) Marker-based estimation of heritability in immortal populations. Genetics 199(2), 379-398.
| Crossref | Google Scholar | PubMed |

Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82(13), 1-26.
| Crossref | Google Scholar |

Lenth RV (2016) Least-Squares Means: the R package lsmeans. Journal of Statistical Software 69(1), 1-33.
| Crossref | Google Scholar |

Lobell DB, Roberts MJ, Schlenker W, Braun N, Little BB, Rejesus RM, Hammer GL (2014) Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science 344(6183), 516-519.
| Crossref | Google Scholar | PubMed |

López J, Way DA, Sadok W (2021) Systemic effects of rising atmospheric vapor pressure deficit on plant physiology and productivity. Global Change Biology 27, 1704-1720.
| Crossref | Google Scholar | PubMed |

Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Journal of Animal Breeding and Genetics 119, 406.

Messina CD, Sinclair TR, Hammer GL, Curan D, Thompson J, Oler Z, Gho C, Cooper M (2015) Limited-transpiration trait may increase maize drought tolerance in the US Corn Belt. Agronomy Journal 107, 1978-1986.
| Crossref | Google Scholar |

Monteith JL (1995) A reinterpretation of stomatal responses to humidity. Plant, Cell & Environment 18, 357-364.
| Crossref | Google Scholar |

Mourtzinis S, Specht JE, Conley SP (2019) Defining optimal soybean sowing dates across the US. Scientific Reports 9, 2800.
| Crossref | Google Scholar | PubMed |

Novick KA, Ficklin DL, Grossiord C, Konings AG, Martínez-Vilalta J, Sadok W, Trugman AT, Williams AP, Wright AJ, Abatzoglou JT, Dannenberg MP, Gentine P, Guan K, Johnston MR, Lowman LEL, Moore DJP, McDowell N (2024) The impacts of rising vapor pressure deficit in natural and managed ecosystems. Plant, Cell & Environment 47, 3561-3589.
| Crossref | Google Scholar |

R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at http://www.r-project.org/

Sadok W, Sinclair TR (2009a) Genetic variability of transpiration response to vapor pressure deficit among soybean cultivars. Crop Science 49, 955-960.
| Crossref | Google Scholar |

Sadok W, Sinclair TR (2009b) Genetic variability of transpiration response to vapor pressure deficit among soybean (Glycine max [L.] Merr.) genotypes selected from a recombinant inbred line population. Field Crops Research 113(2), 156-160.
| Crossref | Google Scholar |

Sadok W, Sinclair TR (2010a) Transpiration response of ‘slow-wilting’ and commercial soybean (Glycine max (L.) Merr.) genotypes to three aquaporin inhibitors. Journal of Experimental Botany 61(3), 821-829.
| Crossref | Google Scholar | PubMed |

Sadok W, Sinclair TR (2010b) Genetic variability of transpiration response of soybean [Glycine max (L.) Merr.] shoots to leaf hydraulic conductance inhibitor AgNO3. Crop Science 50, 1423-1430.
| Crossref | Google Scholar |

Sadok W, Tamang BG (2019) Diversity in daytime and night-time transpiration dynamics in barley indicates adaptation to drought regimes across the Middle-East. Journal of Agronomy and Crop Science 205, 372-384.
| Crossref | Google Scholar |

Sadok W, Schoppach R, Ghanem ME, Zucca C, Sinclair TR (2019) Wheat drought-tolerance to enhance food security in Tunisia, birthplace of the Arab spring. European Journal of Agronomy 107, 1-9.
| Crossref | Google Scholar |

Sadok W, Lopez JR, Zhang Y, Tamang BG, Muehlbauer GJ (2020) Sheathing the blade: significant contribution of sheaths to daytime and nighttime gas exchange in a grass crop. Plant, Cell & Environment 43, 1844-1861.
| Crossref | Google Scholar |

Sadok W, Lopez JR, Smith KP (2021) Transpiration increases under high-temperature stress: potential mechanisms, trade-offs and prospects for crop resilience in a warming world. Plant Cell & Environment 44, 2102-2116.
| Crossref | Google Scholar |

Sarkar S, Shekoofa A, McClure A, Gillman JD (2022) Phenotyping and quantitative trait locus analysis for the limited transpiration trait in an upper-mid south soybean recombinant inbred line population (“Jackson” × “KS4895”): High throughput aquaporin inhibitor screening. Frontiers in Plant Science 12, 779834.
| Crossref | Google Scholar | PubMed |

Schoppach R, Sadok W (2012) Differential sensitivities of transpiration to evaporative demand and soil water deficit among wheat elite cultivars indicate different strategies for drought tolerance. Environmental and Experimental Botany 84, 1-10.
| Crossref | Google Scholar |

Seversike TM, Sermons SM, Sinclair TR, Carter TE, Jr., Rufty TW (2014) Physiological properties of a drought-resistant wild soybean genotype: transpiration control with soil drying and expression of root morphology. Plant and Soil 374, 359-370.
| Crossref | Google Scholar |

Sinclair TR, Hammer GL, van Oosterom EJ (2005) Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate. Functional Plant Biology 32, 945-952.
| Crossref | Google Scholar | PubMed |

Sinclair TR, Zwieniecki MA, Holbrook NM (2008) Low leaf hydraulic conductance associated with drought tolerance in soybean. Physiologia Plantarum 132(4), 446-451.
| Crossref | Google Scholar | PubMed |

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, 475-482.
| Crossref | Google Scholar |

Sinclair TR, Devi J, Shekoofa A, Choudhary S, Sadok W, Vadez V, Riar M, Rufty T (2017) Limited-transpiration response to high vapor pressure deficit in crop species. Plant Science 260, 109-118.
| Crossref | Google Scholar | PubMed |

Song Q, Yan L, Quigley C, Jordan BD, Fickus E, Schroeder S, Song BH, Charles An Y-Q, Hyten D, Nelson R, Rainey K, Beavis WD, Specht J, Diers B, Cregan P (2017) Genetic characterization of the soybean nested association mapping population. The Plant Genome 10, 1-14.
| Crossref | Google Scholar |

Steketee CJ, Sinclair TR, Riar MK, Schapaugh WT, Li Z (2019) Unraveling the genetic architecture for carbon and nitrogen related traits and leaf hydraulic conductance in soybean using genome-wide association analyses. BMC Genomics 20, 811.
| Crossref | Google Scholar | PubMed |

Sun W, Fleisher D, Timlin D, Ray C, Wang Z, Beegum S, Reddy V (2023) Projected long-term climate trends reveal the critical role of vapor pressure deficit for soybean yields in the US Midwest. Science of the Total Environment 878, 162960.
| Crossref | Google Scholar | PubMed |

Tamang BG, Sadok W (2018) Nightly business: Links between daytime canopy conductance, nocturnal transpiration and its circadian control illuminate physiological trade-offs in maize. Environmental and Experimental Botany 148, 192-202.
| Crossref | Google Scholar |

Tamang BG, Schoppach R, Monnens D, Steffenson BJ, Anderson JA, Sadok W (2019) Variability in temperature-independent transpiration responses to evaporative demand correlate with nighttime water use and its circadian control across diverse wheat populations. Planta 250, 115-127.
| Crossref | Google Scholar | PubMed |

Tamang BG, Monnens D, Anderson JA, Steffenson BJ, Sadok W (2022) The genetic basis of transpiration sensitivity to vapor pressure deficit in wheat. Physiologia Plantarum 174(5), e13752.
| Crossref | Google Scholar | PubMed |

Thimijan RW, Heins RD (1983) Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. HortScience 18(6), 818-822.
| Crossref | Google Scholar |

Ye H, Song L, Schapaugh WT, Ali ML, Sinclair TR, Riar MK, Mutava RN, Li Y, Vuong T, Valliyodan B, Neto AP, Klepadlo M, Song Q, Shannon JG, Chen P, Nguyen HT (2020) The importance of slow canopy wilting in drought tolerance in soybean. Journal of Experimental Botany 71(2), 642-652.
| Crossref | Google Scholar | PubMed |

Yuan W, Zheng Y, Piao S, Ciais P, Lombardozzi D, Wang Y, Ryu Y, Chen G, Dong W, Hu Z, Jain AK, Jiang C, Kato E, Li S, Lienert S, Liu S, Nabel JEMS, Qin Z, Quine T, Sitch S, Smith WK, Wang F, Wu C, Xiao Z, Yang S (2019) Increased atmospheric vapor pressure deficit reduces global vegetation growth. Science Advances 5, eaax1396.
| Crossref | Google Scholar |

Zhang K, Kimball JS, Nemani RR, Running SW, Hong Y, Gourley JJ, Yu Z (2015) Vegetation greening and climate change promote multidecadal rises of global land evapotranspiration. Scientific Reports 5, 15956.
| Crossref | Google Scholar | PubMed |