Abstract
Drought stress on reproductive stages constitute a major problem for common bean (Phaseolus vulgaris L.) production because it affects flowering and pod-filling processes which are highly drought-sensitive. In this study, we used a greenhouse experiment to evaluate the response to drought stress in ten highly cultivated Brazilian genotypes in response to moderate intermittent drought during flowering and pod-filling periods (R7 and R8 stages). Morphological, biochemical, physiological and agronomic traits were used to identify tolerant cultivars and elucidate their strategies to cope this stress. The drought intensity index for the experiment reached 0.63. The cultivar IAC Imperador can be defined as a tolerant cultivar, presenting the lowest grain yield reduction (43%) and a reduced drought susceptibility index (0.65). This cultivar elevated their level of proline in roots under stress, which allowed the osmotic adjustment and the maintenance of an intermediate stomata closure during the day, which maintained the intrinsic WUE stable in NS and DS conditions. In addition, this cultivar was able to mobilize the assimilated carbon for the production of pods and grains, evidenced by the high harvest index and the high grain filling index. In this way, IAC Imperador can be used as a check in breeding programs to identify and select lineages with drought tolerance in common bean.
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Abbreviations
- 100GW:
-
100 grains dry weight
- ABA:
-
Abscisic acid
- A N :
-
Net CO2 assimilation rate
- C i :
-
Leaf internal CO2 concentration
- CO2 :
-
Carbon dioxide
- DAE:
-
Days after emergency
- DII:
-
Drought intensity index
- DS:
-
Drought-stressed
- DSI:
-
Drought susceptibility index
- DTI:
-
Drought tolerance index
- E :
-
Transpiration rate
- EUW:
-
Effective use of water
- FGP:
-
Number of failed grains per pod
- GFI:
-
Grain filling index
- GMP:
-
Geometric mean productivity
- g S :
-
Stomatal conductance
- GY:
-
Grain yield per plant
- HI:
-
Harvest index
- Ψw:
-
Water potential
- iWUE:
-
Intrinsic water use efficiency
- LSR:
-
Leaf stem ratio
- MP:
-
Mean productivity
- NS:
-
Non-stressed
- NGP:
-
Number of grains per pod
- NPP:
-
Number of pods per plant
- RCBD:
-
Randomized complete block design
- WUE:
-
Water use efficiency
- WUEinst:
-
Instantaneous WUE
- YRR:
-
Yield reduction rate
- YSI:
-
Yield stability index
References
Ambachew D, Mekbib F, Asfaw A, Beebe SE, Blair MW (2015) Trait associations in common bean genotypes grown under drought stress and field infestation by BSM bean fly. Crop J 3:305–316. doi:10.1016/j.cj.2015.01.006
Andrade ER, Ribeiro VN, Azevedo CV, Chiorato AF, Williams TC, Carbonell SA (2016) Biochemical indicators of drought tolerance in the common bean (Phaseolus vulgaris). Euphytica 210(2):277–289. doi:10.1007/s10681-016-1720-4
Asfaw A, Blair MW (2014) Quantification of drought tolerance in Ethiopian common bean varieties. Agric Sci 5:124–139. doi:10.4236/as.2014.52016
Assefa T, Wu J, Beebe SE, Rao IM, Marcomin D, Claude RJ (2015) Improving adaptation to drought stress in small red common bean: phenotypic differences and predicted genotypic effects on grain yield, yield components and harvest index. Euphytica 203(3):477–489. doi:10.1007/s10681-014-1242-x
Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207
Beebe SE, Rao IM, Cajiao C, Grajales M (2008) Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Sci 48:582–592. doi:10.2135/cropsci2007.07.0404
Beebe SE, Rao IM, Blair MW, Acosta-Gallegos JA (2013) Phenotyping common beans for adaptation to drought. Front Physiol 4:35. doi:10.3389/fphys.2013.00035
Blair MW, Galeano CH, Tovar E, Torres MCM, Castrillon AV, Beebe SE, Rao IM (2012) Development of a Mesoamerican intra-genepool genetic map for quantitative trait loci detection in a drought tolerant × susceptible common bean (Phaseolus vulgaris L.) cross. Mol Breeding 29:71–88. doi:10.1007/s11032-010-9527-9
Blum A (2009) Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Res 112(2):119–123. doi:10.1016/j.fcr.2009.03.009
Blum A (2015) Towards a conceptual ABA ideotype in plant breeding for water limited environments. Funct Plant Biol 42(6):502–513. doi:10.1071/FP14334
Bouslama M, Schapaugh WT (1984) Stress tolerance in soybean: 1. Evaluation of three screening techniques for heat and drought tolerance. Crop Sci 24:933–937
Boyle RK, McAinsh M, Dodd IC (2016) Stomatal closure of Pelargonium × hortorum in response to soil water deficit is associated with decreased leaf water potential only under rapid soil drying. Physiol Plant 156(1):84–96. doi:10.1111/ppl.12346
CGIAR—Consultative Group for International Agricultural Research (2016). http://www.cgiar.org/our-strategy/crop-factsheets/beans/
Chai Q, Gan Y, Zhao C, Xu HL, Waskom RM, Niu Y, Siddique KH (2016) Regulated deficit irrigation for crop production under drought stress. A review. Agron Sustain Dev 36(1):1–21. doi:10.1007/s13593-015-0338-6
Chiorato AF, Carbonell SAM, Carvalho CRL, Barros VLNPD, Borges WLB, Ticelli M, Gallo PB, Finoto EL, Santos NCBD (2012) ‘IAC IMPERADOR’: early maturity” carioca” bean cultivar. Crop Breed Appl Biotechnol 12(4):297–300. doi:10.1590/S1984-70332012000400012
CONAB (2015) Acompanhamento da safra brasileira de grãos. V-3 Safra 2015/2016—N 3—Terceiro levantamento. http://www.conab.gov.br/OlalaCMS/uploads/arquivos/16_01_12_09_00_46_boletim_graos_janeiro_2016.pdf
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55(407):2447–2460. doi:10.1093/jxb/erh277
Cruz CD (2013) Genes: a software package for analysis in experimental statistics and quantitative genetics. Acta Sci Agron 35(3):271–276. doi:10.4025/actasciagron.v35i3.21251
Cuellar-Ortiz SM, Arrieta-Montiel MP, Acosta-Gallegos JA, Covarrubias AA (2008) Relationship between carbohydrate partitioning and drought resistance in common bean. Plant, Cell Environ 31(10):1399–1409. doi:10.1111/j.1365-3040.2008.01853.x
Darkwa K, Ambachew D, Mohammed H, Asfaw A, Blair MW (2016) Evaluation of common bean (Phaseolus vulgaris L.) genotypes for drought stress adaptation in Ethiopia. Crop J 4(5):367–376. doi:10.1016/j.cj.2016.06.007
Daryanto S, Wang L, Jacinthe P-A (2015) Global synthesis of drought effects on food legume production. PLoS ONE 10(6):e0127401. doi:10.1371/journal.pone.0127401
FAO (Food and Agriculture Organization of the United Nations) (2015) About the international year of pulses. http://www.fao.org/pulses-2016/en/
FAOSTAT (2014) Glossary. http://faostat.fao.org/site/375/default.aspx
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212. doi:10.1051/agro:2008021
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2016) Drought stress in grain legumes during reproduction and grain filling. J Agro Crop Sci 203(2): 81–102. doi:10.1111/jac.12169
Fernández F, Gepts P, Lopez M (1982) Etapas de desarrollo de la planta de frijol común. Centro Internacional de Agricultura Tropical, Cali
Fischer R, Maurer R (1978) Drought resistance in spring wheat cultivars. I. Grain yield responses. Crop Pasture Sci 29:897–912
Flexas J (2016) Genetic improvement of leaf photosynthesis and intrinsic water use efficiency in C3 plants: Why so much little success? Plant Sci 251:155–161. doi:10.1016/j.plantsci.2016.05.002
Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35(7):2015–2036. doi:10.1007/s11738-013-1239-4
Heinemann AB, Ramirez-Villegas J, Souza TLP, Didonet AD, Di Stefano JG, Boote KJ, Jarvis A (2016) Drought impact on rainfed common bean production areas in Brazil. Agric For Meteorol 225:57–74. doi:10.1016/j.agrformet.2016.05.010
Kijne JW, Barker R, Molden DJ (eds) (2003) Water productivity in agriculture: limits and opportunities for improvement. CABI, London, p 332
Kishor K, Polavarapu B, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant, Cell Environ 37(2):300–311. doi:10.1111/pce.12157
Lanna AC, Mitsuzono ST, Terra TGR, Vianello RP, de Figueiredo Carvalho MA (2016) Physiological characterization of common bean (Phaseolus vulgaris L.) genotypes, water-stress induced with contrasting response towards drought. Aust J Crop Sci 10(1):1
Levitt J (1972) Responses of plants to environmental stresses. Academic Press, New York, p 698
Medrano H, Tomás M, Martorell S, Flexas J, Hernández E, Rosselló J, Pou A, Escalona J-M, Bota J (2015) From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J 3(3):220–228. doi:10.1016/j.cj.2015.04.002
Moda-Cirino V, Oliari L, Lollato MA, Fonseca Júnior NS (2001) IPR88 Uirapuru -common bean. Crop Breed Appl Biotechnol 1:205–206
Molina JC, Moda-Cirino V, Júnior NDSF, Faria RT, Destro D (2001) Response of common bean cultivars and lines to water stress. Crop Breed Appl Biotechnol 1(4):363–372
Müller BSF, Sakamoto T, Silveira RDD, Zambussi-Carvalho PF, Pereira M, Pappas GJ Jr, Costa MMC, Guimarães CM, Pereira WJ, Brondani C, Vianello-Brondani RP (2014) Differentially expressed genes during flowering and grain filling in common bean (Phaseolus vulgaris) grown under drought stress conditions. Plant Mol Biol Report 32(2):438–451. doi:10.1007/s11105-013-0651-7
Muñoz-Perea CG, Terán H, Allen RG, Wright JL, Westermann DT, Singh SP (2006) Selection for drought resistance in dry bean landraces and cultivars. Crop Sci 46(5):2111–2120. doi:10.2135/cropsci2006.01.0029
Mwenye OJ, van Rensburg L, van Biljon A, van der Merwe R (2016) The role of proline and root traits on selection for drought stress tolerance in soybeans: a review. S Afr J Plant Soil 33(4):1–12. doi:10.1080/02571862.2016.1148786
Namugwanya M, Tenywa JS, Otabbong E, Mubiru DN, Masamba TA (2014) Development of common bean (Phaseolus vulgaris L.) production under low soil phosphorus and drought in Sub-Saharan Africa: a review. J Sustain Dev 7(5):128. doi:10.5539/jsd.v7n5p128
Nezhadahmadi A, Prodhan ZH, Faruq G (2013) Drought tolerance in wheat. Sci World J. doi:10.1155/2013/610721
Omae H, Kumar A, Shono M (2012) Adaptation to high temperature and water deficit in the common bean (Phaseolus vulgaris L.) during the reproductive period. J Bot. Article ID 803413. doi:10.1155/2012/803413
Oya T, Nepomucemo AL, Neumaier N, Farias JRB, Tobita S, Ito O (2004) Drought tolerance characteristics of Brazilian soybean cultivars: evaluation and characterization of drought tolerance of various Brazilian soybean cultivars in the field. Plant Prod Sci 7(2):129–137
Pérez-Vega JC, Blair MW, Monserrate F, Ligarreto GM (2011) Evaluation of an Andean common bean reference collection under drought stress. Agronomía Colombiana 29(1):17–26
Polania JA, Poschenrieder C, Beebe S, Rao IM (2016a) Effective use of water and increased dry matter partitioned to grain contribute to yield of common bean improved for drought resistance. Front Plant Sci. doi:10.3389/fpls.2016.00660
Polania J, Rao IM, Cajiao C, Rivera M, Raatz B, Beebe S (2016b) Physiological traits associated with drought resistance in Andean and Mesoamerican genotypes of common bean (Phaseolus vulgaris L.). Euphytica 210(1):17–29. doi:10.1007/s10681-016-1691-5
Ramirez-Vallejo P, Kelly JD (1998) Traits related to drought resistance in common bean. Euphytica 99:127–136
Rao DE, Chaitanya KV (2016) Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. Biol Plant 60(2):201–218. doi:10.1007/s10535-016-0584-8
Rao I, Beebe S, Polania J, Ricaurte J, Cajiao C, Garcia R, Rivera M (2013) Can tepary bean be a model for improvement of drought resistance in common bean? Afr Crop Sci J 21:265–281
Rosales MA, Ocampo E, Rodríguez-Valentín R, Olvera-Carrillo Y, Acosta-Gallegos J, Covarrubias AA (2012) Physiological analysis of common bean (Phaseolus vulgaris L.) cultivars uncovers characteristics related to terminal drought resistance. Plant Physiol Biochem 56:24–34. doi:10.1016/j.plaphy.2012.04.007
Rosales MA, Cuellar-Ortiz SM, Arrieta-Montiel MP, Acosta-Gallegos J, Covarrubias AA (2013) Physiological traits related to terminal drought resistance in common bean (Phaseolus vulgaris L.). J Sci Food Agric 93:324–331. doi:10.1002/jsfa.5761
Rosielle AA, Hamblin J (1981) Theoretical aspects of selection for yield in stress and non-stress environments. Crop Sci 21(6):943–946
Scholander P, Hammel H, Bradstreet EY, Hemmingsen E (1965) Sap pressure in vascular plants. Science 148:339–346
Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS ONE 7(6):e38554. doi:10.1371/journal.pone.0038554
Singh SP, Teran H, Gutierrez AJ (2001) Registration of SEA 5 and SEA 13 drought tolerant dry bean germplasm. Crop Sci 41(1):276
Singh S, Tripathi DK, Dubey NK, Chauhan DK (2016) Global explicit profiling of water deficit-induced diminutions in agricultural crop sustainability: key emerging trends and challenges., Water stress and crop plants: a sustainable approachWiley, Chichester
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. doi:10.1016/j.tplants.2009.11.009
Szilagyi L (2003) Influence of drought on seed yield components in common bean. Bulg J Plant Physiol 9:320–330
Terán H, Singh SP (2002) Selection for drought resistance in early generations of common bean populations. Can J Plant Sci 82(3):491–497. doi:10.4141/P01-134
Tombesi S, Nardini A, Tommaso F, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2016) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:12449. doi:10.1038/srep12449
Villordo-Pineda E, González-Chavira MM, Giraldo-Carbajo P, Acosta-Gallegos JA, Caballero-Pérez J (2015) Identification of novel drought-tolerant-associated SNPs in common bean (Phaseolus vulgaris). Front Plant Sci. doi:10.3389/fpls.2015.00546
Voleníková M, Tichá I (2001) Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets. Biol Plant 44:161–165
White JW, Castillo JA (1992) Evaluation of diverse shoot genotypes on selected root genotypes of common bean under soil water deficits. Crop Sci 32:762–765
Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell Environ 33(4):510–525. doi:10.1111/j.1365-3040.2009.02052.x
Zadražnik T, Hollung K, Egge-Jacobsen W, Meglič V, Šuštar-Vozlič J (2013) Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J Proteomics 78:254–272. doi:10.1016/j.jprot.2012.09.021
Acknowledgments
The authors are grateful to CNPq, CAPES, Fundação Araucária and UTFPR for financial support.
Author’s contribution
TF, JAM and CCD conceived the study. CCD, MAB, KKK, MHR, DRG, FP, KF, LGW and TF performed the experiment and collected data. CCD, MHR, LGW and TF analysed the data. CCD, TF and LGW wrote the manuscript. All authors read and approved the final manuscript.
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Dipp, C.C., Marchese, J.A., Woyann, L.G. et al. Drought stress tolerance in common bean: what about highly cultivated Brazilian genotypes?. Euphytica 213, 102 (2017). https://doi.org/10.1007/s10681-017-1893-5
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DOI: https://doi.org/10.1007/s10681-017-1893-5