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A Dual Strategy of Breeding for Drought Tolerance and Introducing Drought-Tolerant, Underutilized Crops into Production Systems to Enhance Their Resilience to Water Deficiency

. 2020 Sep 24 ; 9 (10) : . [epub] 20200924

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article, Review

Grant support
40/2015 The Internal Grant Agency, FA, Mendel University in Brno
QK1910197 NAAR
1828 Ministerio de Agricultura y Desarrollo Rural (MADR) of Colombia

Water scarcity is the primary constraint on crop productivity in arid and semiarid tropical areas suffering from climate alterations; in accordance, agricultural systems have to be optimized. Several concepts and strategies should be considered to improve crop yield and quality, particularly in vulnerable regions where such environmental changes cause a risk of food insecurity. In this work, we review two strategies aiming to increase drought stress tolerance: (i) the use of natural genes that have evolved over time and are preserved in crop wild relatives and landraces for drought tolerance breeding using conventional and molecular methods and (ii) exploiting the reservoir of neglected and underutilized species to identify those that are known to be more drought-tolerant than conventional staple crops while possessing other desired agronomic and nutritive characteristics, as well as introducing them into existing cropping systems to make them more resilient to water deficiency conditions. In the past, the existence of drought tolerance genes in crop wild relatives and landraces was either unknown or difficult to exploit using traditional breeding techniques to secure potential long-term solutions. Today, with the advances in genomics and phenomics, there are a number of new tools available that facilitate the discovery of drought resistance genes in crop wild relatives and landraces and their relatively easy transfer into advanced breeding lines, thus accelerating breeding progress and creating resilient varieties that can withstand prolonged drought periods. Among those tools are marker-assisted selection (MAS), genomic selection (GS), and targeted gene editing (clustered regularly interspaced short palindromic repeat (CRISPR) technology). The integration of these two major strategies, the advances in conventional and molecular breeding for the drought tolerance of conventional staple crops, and the introduction of drought-tolerant neglected and underutilized species into existing production systems has the potential to enhance the resilience of agricultural production under conditions of water scarcity.

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Simelton E.S., Fraser E.D.G., Termansen M., Benton T.G., Gosling S.N., South A., Arnell N.W., Challinor A.J., Dougill A.J., Forster P.M.D.F. The socioeconomics of food crop production and climate change vulnerability: A global scale quantitative analysis of how grain crops are sensitive to drought. Food Secur. 2012;4:163–179. doi: 10.1007/s12571-012-0173-4. DOI

Lipiec J., Doussan C., Nosalewicz A., Kondracka K. Effect of drought and heat stresses on plant growth and yield: A review. Int. Agrophysics. 2013;27:463–477. doi: 10.2478/intag-2013-0017. DOI

Turner N. Drought resistance and adaptation to water deficits in crop plants. In: Mussell H., Staples R.C., editors. Stress Physiology in Crop Plants. John Wiley & Sons; New York, NY, USA: 1979. pp. 343–372.

Passioura J.B. Drought and drought tolerance. Plant Growth Regul. 1996;20:79–83. doi: 10.1007/BF00024003. DOI

Castañeda-Álvarez N.P., Khoury C.K., Achicanoy H.A., Bernau V., Dempewolf H., Eastwood R.J., Guarino L., Harker R.H., Jarvis A., Maxted N., et al. Global conservation priorities for crop wild relatives. Nat. Plants. 2016;2:16022. doi: 10.1038/nplants.2016.22. PubMed DOI

Vincent H., Amri A., Castañeda-Álvarez N.P., Dempewolf H., Dulloo E., Guarino L., Hole D.G., Mba C., Toledo A., Maxted N. Modeling of crop wild relative species identifies areas globally for in situ conservation. Commun. Biol. 2019;2:136. doi: 10.1038/s42003-019-0372-z. PubMed DOI PMC

Villa T.C.C., Maxted N., Scholten M., Ford-Lloyd B. Defining and identifying crop landraces. Plant Genet. Resour. 2005;3:373–384. doi: 10.1079/PGR200591. DOI

Xu Y., Skinner D.J., Wu H., Palacios-Rojas N., Araus J.L., Yan J., Gao S., Warburton M.L., Crouch J.H. Advances in maize genomics and their value for enhancing genetic gains from breeding. Int. J. Plant Genom. 2009;2009:1–30. doi: 10.1155/2009/957602. PubMed DOI PMC

Chivenge P., Mabhaudhi T., Modi A.T., Mafongoya P. The potential role of neglected and underutilised crop species as future crops under water scarce conditions in sub-Saharan Africa. Int. J. Environ. Res. Public Health. 2015;12:5685–5711. doi: 10.3390/ijerph120605685. PubMed DOI PMC

Mabhaudhi T., Chimonyo V., Modi A.T. Status of underutilised crops in South Africa: Opportunities for developing research capacity. Sustainibility. 2017;9:1569. doi: 10.3390/su9091569. DOI

Modi A.T., Mabhaudhi T. Final Report of Water Research Commission Project K5/1771//4. Water Research Commission; Pretoria, South Africa: 2013. Water use and drought tolerance of selected traditional and indigenous crops.

Padulosi S., Thompson J., Rudebjer P. Fighting Poverty, Hunger and Malnutrition with Neglected and Underutilized Species (NUS): Needs, Challenges and the Way Forward: Neglected and Underutilized Species. Bioversity International; Rome, Italy: 2013.

Bazile D., Pulvento C., Verniau A., Al-Nusairi M.S., Ba D., Breidy J., Hassan L., Mohammed M.I., Mambetov O., Otambekova M., et al. Worldwide evaluations of quinoa: Preliminary results from post international year of quinoa FAO projects in nine countries. Front. Plant Sci. 2016;7:850. doi: 10.3389/fpls.2016.00850. PubMed DOI PMC

Mustafa M.A., Mayes S., Massawe F. Sustainable Solutions for Food Security. Springer Science and Business Media LLC.; Berlin, Germany: 2019. Crop diversification through a wider use of underutilised crops: A strategy to ensure food and nutrition security in the face of climate change; pp. 125–149.

Harb A., Krishnan A., Ambavaram M.M., Pereira A. Molecular and physiological analysis of drought stress in arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol. 2010;154:1254–1271. doi: 10.1104/pp.110.161752. PubMed DOI PMC

Shabala S., Bose J., Fuglsang A.T., Pottosin I. On a quest for stress tolerance genes: Membrane transporters in sensing and adapting to hostile soils. J. Exp. Bot. 2015;67:1015–1031. doi: 10.1093/jxb/erv465. PubMed DOI

Osakabe Y., Osakabe K., Shinozaki K., Tran L.-S.P. Response of plants to water stress. Front. Plant Sci. 2014;5:86. doi: 10.3389/fpls.2014.00086. PubMed DOI PMC

Ding S., Zhang B., Qin F. Arabidopsis RZFP34/CHYR1, a ubiquitin E3 ligase, regulates stomatal movement and drought tolerance via SnRK2.6-mediated phosphorylation. Plant Cell. 2015;27:3228–3244. doi: 10.1105/tpc.15.00321. PubMed DOI PMC

Wang Y., Noguchi K., Ono N., Inoue S.-I., Terashima I., Kinoshita T. Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth. Proc. Natl. Acad. Sci. USA. 2013;111:533–538. doi: 10.1073/pnas.1305438111. PubMed DOI PMC

Daszkowska-Golec A. Drought Stress Tolerance in Plants. Volume 2. Springer Science and Business Media LLC; Berlin, Germany: 2016. The role of abscisic acid in drought stress: How ABA helps plants to cope with drought stress; pp. 123–151.

Yang J., Zhang G., An J., Li Q., Chen Y., Zhao X., Wu J., Wang Y., Hao Q., Wang W., et al. Expansin gene TaEXPA2 positively regulates drought tolerance in transgenic wheat (Triticum aestivum L.) Plant Sci. 2020;298:110596. doi: 10.1016/j.plantsci.2020.110596. PubMed DOI

Fang Q., Wang X., Wang H., Tang X., Liu C., Yin H., Ye S., Jiang Y., Duan Y., Luo K. The poplar R2R3 MYB transcription factor PtrMYB94 coordinates with abscisic acid signaling to improve drought tolerance in plants. Tree Physiol. 2019;40:46–59. doi: 10.1093/treephys/tpz113. PubMed DOI

Zhong M.-S., Jiang H., Cao Y., Wang Y.-X., You C.-X., Li Y.-Y., Hao Y.-J. MdCER2 conferred to wax accumulation and increased drought tolerance in plants. Plant Physiol. Biochem. 2020;149:277–285. doi: 10.1016/j.plaphy.2020.02.013. PubMed DOI

Virlouvet L., Fromm M. Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol. 2014;205:596–607. doi: 10.1111/nph.13080. PubMed DOI

Grondin A., Rodrigues O., Verdoucq L., Merlot S., Leonhardt N., Maurel C. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell. 2015;27:1945–1954. doi: 10.1105/tpc.15.00421. PubMed DOI PMC

Yang L., Fountain J.C., Wang H., Ni X., Ji P., Lee R.D., Kemerait R.C., Scully B.T., Guo B. Stress sensitivity is associated with differential accumulation of reactive oxygen and nitrogen species in maize genotypes with contrasting levels of drought tolerance. Int. J. Mol. Sci. 2015;16:24791–24819. doi: 10.3390/ijms161024791. PubMed DOI PMC

Laxa M., Liebthal M., Telman W., Chibani K., Dietz K.-J. The role of the plant antioxidant system in drought tolerance. Antioxidants. 2019;8:94. doi: 10.3390/antiox8040094. PubMed DOI PMC

Smékalová V., Doskočilová A., Komis G., Šamaj J. Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol. Adv. 2014;32:2–11. doi: 10.1016/j.biotechadv.2013.07.009. PubMed DOI

Ullah A., Manghwar H., Shaban M., Khan A.H., Akbar A., Ali U., Ali E., Fahad S. Phytohormones enhanced drought tolerance in plants: A coping strategy. Environ. Sci. Pollut. Res. 2018;25:33103–33118. doi: 10.1007/s11356-018-3364-5. PubMed DOI

Liao W.-B., Huang G.-B., Yu J., Zhang M. Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol. Biochem. 2012;58:6–15. doi: 10.1016/j.plaphy.2012.06.012. PubMed DOI

Fang J., Chai C., Qian Q., Li C., Tang J., Sun L., Huang Z., Guo X., Sun C., Liu M., et al. Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J. 2008;54:177–189. doi: 10.1111/j.1365-313X.2008.03411.x. PubMed DOI PMC

Ford-Lloyd B.V., Schmidt M., Armstrong S.J., Barazani O., Engels J., Hadas R., Hammer K., Kell S.P., Kang D., Khoshbakht K., et al. Crop Wild Relatives—Undervalued, underutilized and under threat? Bioscience. 2011;61:559–565. doi: 10.1525/bio.2011.61.7.10. DOI

Dempewolf H., Baute G., Anderson J., Kilian B., Smith C., Guarino L. Past and future use of wild relatives in crop breeding. Crop. Sci. 2017;57:1070–1082. doi: 10.2135/cropsci2016.10.0885. DOI

Mammadov J., Buyyarapu R., Guttikonda S.K., Parliament K., Abdurakhmonov I.Y., Kumpatla S.P. Wild relatives of maize, rice, cotton, and soybean: Treasure troves for tolerance to biotic and abiotic stresses. Front. Plant Sci. 2018;9:886. doi: 10.3389/fpls.2018.00886. PubMed DOI PMC

Ludwig F., Rosenthal D.M., Johnston J.A., Kane N.C., Gross B.L., Lexer C., Dudley S.A., Rieseberg L.H., Donovan L.A. Selection on leaf ecophysiological traits in a desert hybrid helianthus species and early-generation hybrids. Evolution. 2004;58:2682–2692. doi: 10.1111/j.0014-3820.2004.tb01621.x. PubMed DOI PMC

Ndjiondjop M.N., Manneh B., Cissoko M., Dramé N., Kakaï R.G., Bocco R., Baimey H., Wopereis M. Drought resistance in an interspecific backcross population of rice (Oryza spp.) derived from the cross WAB56-104 (O. sativa)×CG14 (O. glaberrima) Plant Sci. 2010;179:364–373. doi: 10.1016/j.plantsci.2010.06.006. DOI

Budak H., Kantar M., Kurtoglu K.Y. Drought tolerance in modern and wild wheat. Sci. World J. 2013;2013:1–16. doi: 10.1155/2013/548246. PubMed DOI PMC

Alpha Y., Kureh I., Menkir A., Kartung P., Tarfa B., Amaza P. Participatory on-farm evaluation of the performance of drought-tolerant maize varieties in the Guinea savannas of Nigeria. Int. J. Food Agric. Environ. 2006;4:192–196.

Xu J., Yuan Y., Xu Y., Zhang G., Guo X.-S., Wu F., Wang Q., Rong T., Pan G., Cao M., et al. Identification of candidate genes for drought tolerance by whole-genome resequencing in maize. BMC Plant Biol. 2014;14:83. doi: 10.1186/1471-2229-14-83. PubMed DOI PMC

Al Sharari S., Alsadon A., Alharbi A. Evaluation of drought tolerance of potato cultivars under greenhouse conditions. Acta Hortic. 2007;747:67–74. doi: 10.17660/ActaHortic.2007.747.5. DOI

International Potato Center (CIP) Annual Report CIP 1993–1994. CIP; Lima, Peru: 1994. p. 192.

Monneveux P., Ramirez D.A., Pino M.-T. Drought tolerance in potato (S. tuberosum L.) Plant Sci. 2013;205:76–86. doi: 10.1016/j.plantsci.2013.01.011. PubMed DOI

Rolando J., Ramirez D.A., Yactayo W., Monneveux P., Quiroz R. Leaf greenness as a drought tolerance related trait in potato (Solanum tuberosum L.) Environ. Exp. Bot. 2015;110:27–35. doi: 10.1016/j.envexpbot.2014.09.006. DOI

Sharma N., Rawal S., Kadian M., Arya S., Bonierbale M., Singh B. Evaluation of advanced potato clones for drought tolerance in arid zone in Rajasthan, India. Potato J. 2014;41:189–193.

Reyes L. Making rice less thirsty. Rice Today. 2009;8:12–15.

Singh A., Singh A.K., Singh V., Singh N., Singh V.N., Shamim M., Vikram P., Singh S. Genetic variability among traits associated with grain yield of rice (Oryza sativa L.) exposed to drought at flowering stage. Afr. J. Agric. Res. 2014;9:1252–1264.

Zheng X.-G., Chen L., Lou Q.-J., Xia H., Li M.-S., Luo L. Changes in DNA methylation pattern at two seedling stages in water saving and drought-resistant rice variety after drought stress domestication. Rice Sci. 2014;21:262–270. doi: 10.1016/S1672-6308(13)60194-8. DOI

Liu L., Lafitte R., Guan D. Wild Oryza species as potential sources of drought-adaptive traits. Euphytica. 2004;138:149–161. doi: 10.1023/B:EUPH.0000046801.27042.14. DOI

Thanh P.T., Sripichitt P., Chanprame S., Peyachoknagu S. Transfer of drought resistant character from wild rice (Oryza meridionalis and Oryza nivara) to cultivated rice (Oryza sativa L.) by backcrossing and immature embryo culture. Kasetsar J. 2006;40:582–594.

Cia M., Guimaraes A., Medici L.O., Chabregas S., Azevedo R. Antioxidant responses to water deficit by drought-tolerant and -sensitive sugarcane varieties. Ann. Appl. Biol. 2012;161:313–324. doi: 10.1111/j.1744-7348.2012.00575.x. DOI

Da Costa M.L.M., Amorim L.L.B., Onofre A.V.C., De Melo L.J.O.T., De Oliveira M.B.M., De Carvalho R., Benko-Iseppon A.M. Assessment of genetic diversity in contrasting sugarcane varieties using inter-simple sequence repeat (ISSR) markers. Am. J. Plant Sci. 2011;2:425–432. doi: 10.4236/ajps.2011.23048. DOI

Ishaq M.N., Olaoye G., Akinsanya T.O. Screening sugar-cane germplasm for drought tolerance in Nigeria. Plant Genetic Resources Newsletter. 2008;154:48–54.

Srivastava M.K., Li C.N., Li Y.R. Development of sequence characterized amplified region (SCAR) marker for identifying drought tolerant sugarcane genotypes. Aust. J. Crop. Sci. 2012;6:763–767.

Mohanan K. Breeding for special purposes. In: Mohanan K.V., editor. Essentials of Plant Breeding. Prentice-Hall of India Pvt Limited; New Delhi, India: 2010. p. 107.

Finkel E. Richard Richards profile: Making every drop count in the buildup to a blue revolution. Science. 2009;323:1004–1005. doi: 10.1126/science.323.5917.1004. PubMed DOI

Sohail Q., Inoue T., Tanaka H., Eltayeb A.E., Matsuoka Y., Tsujimoto H. Applicability of Aegilops tauschii drought tolerance traits to breeding of hexaploid wheat. Breed. Sci. 2011;61:347–357. doi: 10.1270/jsbbs.61.347. PubMed DOI PMC

Turyagyenda L.F., Kizito E.B., Ferguson M., Baguma Y., Agaba M., Harvey J., Osiru D.S.O. Physiological and molecular characterization of drought responses and identification of candidate tolerance genes in cassava. AoB Plants. 2013;5:plt007. doi: 10.1093/aobpla/plt007. PubMed DOI PMC

Nassar N., Abreu L., Teodoro D., Graciano-Ribeiro D. Drought tolerant stem anatomy characteristics in Manihot esculenta (Euphorbiaceae) and a wild relative. Genet. Mol. Res. 2010;9:1023–1031. doi: 10.4238/vol9-2gmr800. PubMed DOI

Narina S., Jasti M., Buyyarapu R., Bhattacharjee R. Manihot. In: Kole C., editor. Wild Crop Relatives Genomic and Breeding Resources Industrial Crops. Springer; Berlin/Heidelberg, Germany: 2011. pp. 133–156.

Chavez R., Reyes R., Roca W. In vitro culture for the conservation of wild Manihot species. In: Mujeeb-Kazi A., Sitch L., editors. Review of Advances in Plant Biotechnology 1985–1988. CYMMYT and IRRI; Ciudad de México, Mexico: 1989. pp. 301–307.

Huang L., Zhang F., Wang W., Zhou Y., Fu B., Li Z. Comparative transcriptome sequencing of tolerant rice introgression line and its parents in response to drought stress. BMC Genom. 2014;15:1–16. doi: 10.1186/1471-2164-15-1026. PubMed DOI PMC

Khoury C.K., Bjorkman A., Dempewolf H., Ramirez-Villegas J., Guarino L., Jarvis A., Rieseberg L.H., Struik P.C. Increasing homogeneity in global food supplies and the implications for food security. Proc. Natl. Acad. Sci. USA. 2014;111:4001–4006. doi: 10.1073/pnas.1313490111. PubMed DOI PMC

Mayes S., Massawe F., Alderson P.G., Roberts J.A., Azam-Ali S.N., Hermann M. The potential for underutilized crops to improve security of food production. J. Exp. Bot. 2011;63:1075–1079. doi: 10.1093/jxb/err396. PubMed DOI

Boote K.J., Ibrahim A.M.H., Lafitte R., McCulley R., Messina C.D., Murray S.C., Specht J.E., Taylor S., Westgate M.E., Glasener K., et al. Position statement on crop adaptation to climate change. Crop. Sci. 2011;51:2337–2343. doi: 10.2135/cropsci2011.07.0369. DOI

Bose J., Rodrigo-Moreno A., Lai D., Xie Y., Shen W., Shabala S. Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Ann. Bot. 2014;115:481–494. doi: 10.1093/aob/mcu219. PubMed DOI PMC

Yang A., Akhtar S.S., Amjad M., Iqbal S., Jacobsen S.-E. Growth and physiological responses of quinoa to drought and temperature stress. J. Agron. Crop. Sci. 2016;202:445–453. doi: 10.1111/jac.12167. DOI

Shao H., Yong B., Xu P., Zheng H., Liao R., Wang X., Li X., Zhang L., Shen J. Phytoene synthase gene (PSY) from sweet potato (Ipomoea batatas Lam) enhances tolerance to abiotic stress. Braz. Arch. Biol. Technol. 2018;61:e18160558. doi: 10.1590/1678-4324-2018160558. DOI

Park S., Kim H.S., Jung Y.J., Kim S.H., Ji C.Y., Wang Z., Jeong J.C., Lee H.-S., Lee S.Y., Kwak S.-S. Orange protein has a role in phytoene synthase stabilization in sweetpotato. Sci. Rep. 2016;6:33563. doi: 10.1038/srep33563. PubMed DOI PMC

Fang Z., Xu X., Gao J., Wang P., Liu Z., Feng B. Characterization of FeDREB1 promoter involved in cold- and drought-inducible expression from common buckwheat (Fagopyrum esculentum) Genet. Mol. Res. 2015;14:7990–8000. doi: 10.4238/2015.July.17.7. PubMed DOI

Wu Q., Zhao G., Bai X., Zhao W., Xiang D., Wan Y., Wu X., Sun Y., Tan M., Peng L., et al. Characterization of the transcriptional profiles in common buckwheat (Fagopyrum esculentum) under PEG-mediated drought stress. Electron. J. Biotechnol. 2019;39:42–51. doi: 10.1016/j.ejbt.2019.03.005. DOI

Khoury C.K., Achicanoy H.A., Bjorkman A., Navarro-Racines C., Guarino L., Flores-Palacios X., Engels J.M.M., Wiersema J.H., Dempewolf H., Sotelo S., et al. Origins of food crops connect countries worldwide. Proc. R. Soc. B: Biol. Sci. 2016;283:20160792. doi: 10.1098/rspb.2016.0792. DOI

Risi C., Galwey N.W. The Chenopodium grains of the Andes: Inca crops for modern agriculture. Adv. Appl. Biol. 1984;10:145–216.

Jacobsen S.-E. The scope for adaptation of quinoa in Northern Latitudes of Europe. J. Agron. Crop. Sci. 2017;203:603–613. doi: 10.1111/jac.12228. DOI

International Union for the Protection of New Varieties of Plants (UPOV) 2020 PLUTO: Plant Variety Database. [(accessed on 2 September 2020)]; Available online: https://www.upov.int/pluto/en/

Di Fabio A., Parraga G. Origin, Production and Utilization of Pseudocereals. Wiley; Hoboken, NJ, USA: 2017. pp. 1–27.

Oumar I., Mariac C., Pham J.-L., Vigouroux Y. Phylogeny and origin of pearl millet (Pennisetum glaucum [L.] R. Br) as revealed by microsatellite loci. Theor. Appl. Genet. 2008;117:489–497. doi: 10.1007/s00122-008-0793-4. PubMed DOI

Zhou M., Tang Y., Deng X., Ruan C., Kreft I., Tang Y., Wu Y. Overview of buckwheat resources in the world. In: Zhou M., Kreft I., Suvorova G., Tang Y., Wu Y., editors. Buckwheat Germplasm in the World. Academic Press; London, UK: 2018. pp. 1–7.

Padulosi S., Ng N.Q. Origin, taxonomy, and morphology of Vigna unguiculata (L.) Walp. In: Singh B.B., Mohan Raj D.R., Dashiell K.E., Jackai L.E., editors. Advances in Cowpea Research. Sayce Publishing; Devon, UK: 1997. pp. 1–12.

Muñoz-Rodríguez P., Carruthers T., Wood J.R., Williams B.R., Weitemier K., Kronmiller B., Ellis D., Anglin N.L., Longway L., Harris S.A., et al. Reconciling conflicting phylogenies in the origin of sweet potato and dispersal to polynesia. Curr. Biol. 2018;28:1246–1256.e12. doi: 10.1016/j.cub.2018.03.020. PubMed DOI

Atchison G.W., Nevado B., Eastwood R.J., Contreras-Ortiz N., Reynel C., Madriñán S., Filatov D.A., Hughes C.E. Lost crops of the Incas: Origins of domestication of the Andean pulse crop tarwi, Lupinus mutabilis. Am. J. Bot. 2016;103:1592–1606. doi: 10.3732/ajb.1600171. PubMed DOI

Singh M., Malhotra N., Sharma K. Buckwheat (Fagopyrum sp.) genetic resources: What can they contribute towards nutritional security of changing world? Genet. Resour. Crop. Evol. 2020;67:1–20. doi: 10.1007/s10722-020-00961-0. DOI

Cuellar-Ortiz S.M., Arrieta-Montiel M.D.L.P., Acosta-Gallegos J., Covarrubias A.A. Relationship between carbohydrate partitioning and drought resistance in common bean. Plant Cell Environ. 2008;31:1399–1409. doi: 10.1111/j.1365-3040.2008.01853.x. PubMed DOI

Li L., Zhang Q., Huang D. A review of imaging techniques for plant phenotyping. Sensors. 2014;14:20078–20111. doi: 10.3390/s141120078. PubMed DOI PMC

McAusland L., Davey P.A., Kanwal N., Baker N.R., Lawson T. A novel system for spatial and temporal imaging of intrinsic plant water use efficiency. J. Exp. Bot. 2013;64:4993–5007. doi: 10.1093/jxb/ert288. PubMed DOI PMC

Takahashi S., Monda K., Negi J., Konishi F., Ishikawa S., Hashimoto-Sugimoto M., Gotô N., Iba K. Natural variation in stomatal responses to environmental changes among arabidopsis thaliana ecotypes. PLoS ONE. 2015;10:e0117449. doi: 10.1371/journal.pone.0117449. PubMed DOI PMC

Kim D.M., Zhang H., Zhou H., Du T., Wu Q., Mockler T.C., Berezin M. Highly sensitive image-derived indices of water-stressed plants using hyperspectral imaging in SWIR and histogram analysis. Sci. Rep. 2015;5:15919. doi: 10.1038/srep15919. PubMed DOI PMC

Parent B., Shahinnia F., Maphosa L., Berger B., Rabie H., Chalmers K., Kovalchuk A., Langridge P., Fleury D. Combining field performance with controlled environment plant imaging to identify the genetic control of growth and transpiration underlying yield response to water-deficit stress in wheat. J. Exp. Bot. 2015;66:5481–5492. doi: 10.1093/jxb/erv320. PubMed DOI PMC

Humplík J.F., Lazár D., Husičková A., Spíchal L. Automated phenotyping of plant shoots using imaging methods for analysis of plant stress responses—A review. Plant Methods. 2015;11:1–10. doi: 10.1186/s13007-015-0072-8. PubMed DOI PMC

Farooq M.A., Wahid A., Kobayashi N., Fujita D., Basra S.M.A. Plant drought stress: Effects, mechanisms and management. Agron. Sustain. Dev. 2009;29:185–212. doi: 10.1051/agro:2008021. DOI

Prince S., Mutava R.N., Nguyen N., Pathan S.M., Shannon G.J., Murphy M., Zhang Z., Kim Y.H., Valliyodan B., Nguyen H.T. Evaluation of high yielding soybean germplasm under water limitation. J. Integr. Plant Biol. 2015;58:475–491. doi: 10.1111/jipb.12378. PubMed DOI

Das A., Schneider H.M., Burridge J.D., Ascanio A.K.M., Wojciechowski T., Topp C.N., Lynch J.P., Weitz J.S., Bucksch A. Digital imaging of root traits (DIRT): A high-throughput computing and collaboration platform for field-based root phenomics. Plant Methods. 2015;11:51. doi: 10.1186/s13007-015-0093-3. PubMed DOI PMC

Cai J., Zeng Z., Connor J.N., Huang C.Y., Melino V.J., Kumar P., Miklavcic S.J. RootGraph: A graphic optimization tool for automated image analysis of plant roots. J. Exp. Bot. 2015;66:6551–6562. doi: 10.1093/jxb/erv359. PubMed DOI PMC

Kumar P., Cai J., Miklavcic S.J. A complete system for 3D reconstruction of roots for phenotypic analysis. Adv. Exp. Med. Biol. 2014;823:249–270. doi: 10.1007/978-3-319-10984-8_14. PubMed DOI

Sallam A., Alqudah A.M., Dawood M.F.A., Baenziger P.S., Börner A. Drought stress tolerance in wheat and barley: Advances in physiology, breeding and genetics research. Int. J. Mol. Sci. 2019;20:3137. doi: 10.3390/ijms20133137. PubMed DOI PMC

Mohammadi R. Breeding for increased drought tolerance in wheat: A review. Crop. Pasture Sci. 2018;69:223–241. doi: 10.1071/CP17387. DOI

Khan A., Sovero V., Gemenet D.C. Genome-assisted breeding for drought resistance. Curr. Genom. 2016;17:330–342. doi: 10.2174/1389202917999160211101417. PubMed DOI PMC

Upadhyay J., Joshi R., Singh B., Bohra A., Vijayan R., Bhatt M., Bisht S.P.S., Wani S.H. Application of Bioinformatics in Understanding of Plant Stress Tolerance. Springer Science and Business Media LLC; Berlin, Germany: 2017. pp. 347–374.

Sharma V., Sarkar I.N. Bioinformatics opportunities for identification and study of medicinal plants. Briefings Bioinform. 2012;14:238–250. doi: 10.1093/bib/bbs021. PubMed DOI PMC

Blum A. Genomics for drought resistance—Getting down to earth. Funct. Plant Biol. 2014;41:1191–1198. doi: 10.1071/FP14018. PubMed DOI

Nuccio M.L., Wu J., Mowers R., Zhou H.-P., Meghji M., Primavesi L.F., Paul M.J., Chen X., Gao Y., Haque E., et al. Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat. Biotechnol. 2015;33:862–869. doi: 10.1038/nbt.3277. PubMed DOI

Daszkowska-Golec A., Skubacz A., Sitko K., Słota M., Kurowska M., Szarejko I. Mutation in barley ERA1 (Enhanced Response to ABA1) gene confers better photosynthesis efficiency in response to drought as revealed by transcriptomic and physiological analysis. Environ. Exp. Bot. 2018;148:12–26. doi: 10.1016/j.envexpbot.2018.01.003. DOI

Joshi R., Wani S.H., Singh B., Bohra A., Dar Z.A., Lone A., Pareek A., Singla-Pareek S.L. Transcription factors and plants response to drought stress: Current understanding and future directions. Front. Plant Sci. 2016;7:1029. doi: 10.3389/fpls.2016.01029. PubMed DOI PMC

Zhang L., Zhao G., Xia C., Jia J., Liu X., Kong X. A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis. J. Exp. Bot. 2012;63:5873–5885. doi: 10.1093/jxb/ers237. PubMed DOI

Jangale B.L., Chaudhari R.S., Azeez A., Sane P.V., Sane A.P., Krishna B. Independent and combined abiotic stresses affect the physiology and expression patterns of DREB genes differently in stress-susceptible and resistant genotypes of banana. Physiol. Plant. 2018;165:303–318. doi: 10.1111/ppl.12837. PubMed DOI

Bundó M., Coca M.A. Calcium-dependent protein kinase OsCPK10 mediates both drought tolerance and blast disease resistance in rice plants. J. Exp. Bot. 2017;68:2963–2975. doi: 10.1093/jxb/erx145. PubMed DOI PMC

Mitula F., Tajdel M., Cieśla A., Kasprowicz-Maluśki A., Kulik A., Babula-Skowronska D., Michalak M., Dobrowolska G., Sadowski J., Ludwików A. Arabidopsis ABA-activated kinase MAPKKK18 is regulated by protein phosphatase 2C ABI1 and the ubiquitin-proteasome pathway. Plant Cell Physiol. 2015;56:2351–2367. doi: 10.1093/pcp/pcv146. PubMed DOI PMC

Samajova O., Plihal O., Al-Yousif M., Hirt H., Šamaj J. Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Biotechnol. Adv. 2013;31:118–128. doi: 10.1016/j.biotechadv.2011.12.002. PubMed DOI

Wang B., Li Z., Ran Q., Li P., Peng Z., Zhang J. ZmNF-YB16 overexpression improves drought resistance and yield by enhancing photosynthesis and the antioxidant capacity of maize plants. Front. Plant Sci. 2018;9:709. doi: 10.3389/fpls.2018.00709. PubMed DOI PMC

Wu G., Zhao Y., Shen R., Wang B., Xie Y., Ma X., Zheng Z., Wang H. Characterization of maize phytochrome-interacting factors in light signaling and photomorphogenesis. Plant Physiol. 2019;181:789–803. doi: 10.1104/pp.19.00239. PubMed DOI PMC

Gao Y., Jiang W., Dai Y., Xiao N., Zhang C., Li H., Lu Y., Wu M., Tao X., Deng D., et al. A maize phytochrome-interacting factor 3 improves drought and salt stress tolerance in rice. Plant Mol. Biol. 2015;87:413–428. doi: 10.1007/s11103-015-0288-z. PubMed DOI

Khan S., Anwar S., Yu S., Sun M., Yang Z., Gao Z.-Q. Development of drought-tolerant transgenic wheat: Achievements and limitations. Int. J. Mol. Sci. 2019;20:3350. doi: 10.3390/ijms20133350. PubMed DOI PMC

Yang S., Vanderbeld B., Wan J., Huang Y. Narrowing down the targets: Towards successful genetic engineering of drought-tolerant crops. Mol. Plant. 2010;3:469–490. doi: 10.1093/mp/ssq016. PubMed DOI

Gupta P.K., Balyan H.S., Gahlaut V. QTL analysis for drought tolerance in wheat: Present status and future possibilities. Agronomy. 2017;7:5. doi: 10.3390/agronomy7010005. DOI

Shan Q., Wang Y., Li J., Zhang Y., Chen K., Liang Z., Zhang K., Liu J., Xi J.J., Qiu J., et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 2013;31:686–688. doi: 10.1038/nbt.2650. PubMed DOI

Yin F., Gao J., Liu M., Qin C., Zhang W., Yang A., Xia M., Zhang Z., Shen Y., Lin H., et al. Genome-wide analysis of Water-stress-responsive microRNA expression profile in tobacco roots. Funct. Integr. Genom. 2014;14:319–332. doi: 10.1007/s10142-014-0365-4. PubMed DOI

Saad A.S.I., Li X., Li H.-P., Huang T., Gao C.-S., Guo M.-W., Cheng W., Zhao G.-Y., Liao Y.-C. A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses. Plant Sci. 2013;203:33–40. doi: 10.1016/j.plantsci.2012.12.016. PubMed DOI

Jia T.-J., Jing-Jing L., Wang L.-F., Cao Y.-Y., Ma J., Wang H., Zhang D.-F., Li H.-Y. Evaluation of drought tolerance in ZmVPP1-overexpressing transgenic inbred maize lines and their hybrids. J. Integr. Agric. 2020;19:2177–2187. doi: 10.1016/S2095-3119(19)62828-5. DOI

Szalonek M., Sierpien B., Rymaszewski W., Gieczewska K., Garstka M., Lichocka M., Sass L., Paul K., Vass I., Vanková R., et al. Potato annexin STANN1 promotes drought tolerance and mitigates light stress in transgenic solanum tuberosum L. plants. PLoS ONE. 2015;10:e0132683. doi: 10.1371/journal.pone.0132683. PubMed DOI PMC

You J., Hu H., Xiong L. An ornithine δ-aminotransferase gene OsOAT confers drought and oxidative stress tolerance in rice. Plant Sci. 2012;197:59–69. doi: 10.1016/j.plantsci.2012.09.002. PubMed DOI

De Souza W.R., Oliveira N.G., Vinecky F., Ribeiro A.P., Basso M.F., Casari R.A.D.C.N., Cunha B.A.D.B., Duarte K.E., Santiago T.R., Martins P.K., et al. Field evaluation of At DREB 2A CA overexpressing sugarcane for drought tolerance. J. Agron. Crop. Sci. 2019;205:545–553. doi: 10.1111/jac.12341. DOI

Ayadi M., Brini F., Masmoudi K. Overexpression of a wheat aquaporin gene, TdPIP2;1, enhances salt and drought tolerance in transgenic durum wheat cv. maali. Int. J. Mol. Sci. 2019;20:2389. doi: 10.3390/ijms20102389. PubMed DOI PMC

Wei Y., Liu W., Hu W., Yan Y., Shi H. The chaperone MeHSP90 recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava. New Phytol. 2020;226:476–491. doi: 10.1111/nph.16346. PubMed DOI

Li Y., Chen Q., Nan H., Li X., Lu S., Zhao X., Liu B., Guo C., Kong F., Cao D. Overexpression of GmFDL19 enhances tolerance to drought and salt stresses in soybean. PLoS ONE. 2017;12:e0179554. doi: 10.1371/journal.pone.0179554. PubMed DOI PMC

Fan Y., Shabala S., Ma Y., Xu R., Zhou M. Using QTL mapping to investigate the relationships between abiotic stress tolerance (drought and salinity) and agronomic and physiological traits. BMC Genom. 2015;16:43. doi: 10.1186/s12864-015-1243-8. PubMed DOI PMC

Wehner G., Balko C., Enders M.M., Humbeck K., Ordon F. Identification of genomic regions involved in tolerance to drought stress and drought stress induced leaf senescence in juvenile barley. BMC Plant Biol. 2015;15:125. doi: 10.1186/s12870-015-0524-3. PubMed DOI PMC

Uga Y., Sugimoto K., Ogawa S., Rane J., Ishitani M., Hara N., Kitomi Y., Inukai Y., Ono K., Kanno N., et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 2013;45:1097–1102. doi: 10.1038/ng.2725. PubMed DOI

Technow F., Messina C.D., Totir L.R., Cooper M. Integrating crop growth models with whole genome prediction through approximate bayesian computation. PLoS ONE. 2015;10:e0130855. doi: 10.1371/journal.pone.0130855. PubMed DOI PMC

Ghorbani R., Alemzadeh A., Razi H. Microarray analysis of transcriptional responses to salt and drought stress in Arabidopsis thaliana. Heliyon. 2019;5:e02614. doi: 10.1016/j.heliyon.2019.e02614. PubMed DOI PMC

Hassani-Pak K., Singh A., Brandizi M., Hearnshaw J., Amberkar S., Phillips A.L., Doonan J.H., Rawlings C.J. KnetMiner: A comprehensive approach for supporting evidence-based gene discovery and complex trait analysis across species. bioRxiv. 2020;4:017004. PubMed PMC

Noraziyah A.A.S., Swamy B.P.M., Wickneswari R., Cruz M.T.S., Raman A., Kumar A. Marker assisted pyramiding of drought yield QTLs into a popular Malaysian rice cultivar, MR219. BMC Genet. 2016;17:30. doi: 10.1186/s12863-016-0334-0. PubMed DOI PMC

Lopes M.S., El-Basyoni I.S., Baenziger P.S., Singh S., Royo C., Ozbek K., Aktas H., Ozer E., Ozdemir F., Manickavelu A., et al. Exploiting genetic diversity from landraces in wheat breeding for adaptation to climate change. J. Exp. Bot. 2015;66:3477–3486. doi: 10.1093/jxb/erv122. PubMed DOI

Merchuk-Ovnat L., Barak V., Fahima T., Ordon F., Lidzbarsky G.A., Krugman T., Saranga Y. Ancestral QTL alleles from wild emmer wheat improve drought resistance and productivity in modern wheat cultivars. Front. Plant Sci. 2016;7:452. doi: 10.3389/fpls.2016.00452. PubMed DOI PMC

Alqudah A.M., Sallam A., Baenziger P.S., Börner A. GWAS: Fast-forwarding gene identification and characterization in temperate Cereals: Lessons from Barley—A review. J. Adv. Res. 2020;22:119–135. doi: 10.1016/j.jare.2019.10.013. PubMed DOI PMC

Gupta M., Chawla V., Garg P., Yadav N., Munjal R., Sharma B. Genetic analysis of yield and heat stress related traits in wheat (Triticum aestivum L. em. Thell) using microsatellite markers. J. Appl. Nat. Sci. 2015;7:739–744. doi: 10.31018/jans.v7i2.676. DOI

Qaseem M.F., Qureshi R., Muqaddasi Q.H., Shaheen H., Kousar R., Röder M.S. Genome-wide association mapping in bread wheat subjected to independent and combined high temperature and drought stress. PLoS ONE. 2018;13:e0199121. doi: 10.1371/journal.pone.0199121. PubMed DOI PMC

Hou S., Zhu G., Li Y., Li W., Fu J., Niu E., Li L., Zhang D., Guo W. Genome-wide association studies reveal genetic variation and candidate genes of drought stress related traits in cotton (Gossypium hirsutum L.) Front. Plant Sci. 2018;9:9. doi: 10.3389/fpls.2018.01276. PubMed DOI PMC

Kadam N.N., Struik P.C., Rebolledo M.C., Yin X., Jagadish S.V.K. Genome-wide association reveals novel genomic loci controlling rice grain yield and its component traits under water-deficit stress during the reproductive stage. J. Exp. Bot. 2018;69:4017–4032. doi: 10.1093/jxb/ery186. PubMed DOI PMC

Yuan Y., Cairns J.E., Babu R., Gowda M., Makumbi D., Magorokosho C., Zhang A., Liu Y., Wang N., Hao Z., et al. Genome-wide association mapping and genomic prediction analyses reveal the genetic architecture of grain yield and flowering time under drought and heat stress conditions in maize. Front. Plant Sci. 2019;9:9. doi: 10.3389/fpls.2018.01919. PubMed DOI PMC

Gurgul A., Miksza-Cybulska A., Szmatoła T., Jasielczuk I., Piestrzynska-Kajtoch A., Fornal A., Semik-Gurgul E., Bugno-Poniewierska M. Genotyping-by-sequencing performance in selected livestock species. Genomics. 2019;111:186–195. doi: 10.1016/j.ygeno.2018.02.002. PubMed DOI

Ray S., Satya P. Next generation sequencing technologies for next generation plant breeding. Front. Plant Sci. 2014;5:367. doi: 10.3389/fpls.2014.00367. PubMed DOI PMC

Wang X., Xu Y., Hu Z., Yang Z. Genomic selection methods for crop improvement: Current status and prospects. Crop. J. 2018;6:330–340. doi: 10.1016/j.cj.2018.03.001. DOI

Zhao Y., Gowda M., Liu W., Würschum T., Maurer H.P., Longin F.H., Ranc N., Reif J.C. Accuracy of genomic selection in European maize elite breeding populations. Theor. Appl. Genet. 2011;124:769–776. doi: 10.1007/s00122-011-1745-y. PubMed DOI

Bao Y., Vuong T., Meinhardt C., Tiffin P., Denny R., Chen S., Nguyen H.T., Orf J.H., Young N.D. Potential of association mapping and genomic selection to explore PI 88788 derived soybean cyst nematode resistance. Plant Genome. 2014;7:1–13. doi: 10.3835/plantgenome2013.11.0039. DOI

Lorenzana R.E., Bernardo R. Accuracy of genotypic value predictions for marker-based selection in biparental plant populations. Theor. Appl. Genet. 2009;120:151–161. doi: 10.1007/s00122-009-1166-3. PubMed DOI

Spindel J., Begum H., Akdemir D., Virk P., Collard B.C., Redoña E., Atlin G., Jannink J.-L., McCouch S.R. Genomic selection and association mapping in rice (Oryza sativa): Effect of trait genetic architecture, training population composition, marker number and statistical model on accuracy of rice genomic selection in elite, tropical rice breeding lines. PLoS Genet. 2015;11:e1004982. doi: 10.1371/journal.pgen.1004982. PubMed DOI PMC

Sallam A.H., Endelman J.B., Jannink J.-L., Smith K.P. Assessing genomic selection prediction accuracy in a dynamic barley breeding population. Plant Genome. 2015;8:1–15. doi: 10.3835/plantgenome2014.05.0020. PubMed DOI

Cerrudo D., Cao S., Yuan Y., Martínez C., Suarez E.A., Babu R., Zhang X., Trachsel S. Genomic selection outperforms marker assisted selection for grain yield and physiological traits in a maize doubled haploid population across water treatments. Front. Plant Sci. 2018;9:366. doi: 10.3389/fpls.2018.00366. PubMed DOI PMC

Shikha M., Kanika A., Rao A.R., Mallikarjuna M.G., Gupta H.S., Nepolean T. Genomic selection for drought tolerance using genome-wide SNPs in maize. Front. Plant Sci. 2017;8:550. doi: 10.3389/fpls.2017.00550. PubMed DOI PMC

Li Y., Ruperao P., Batley J., Edwards D., Khan T., Colmer T.D., Pang J., Siddique K.H.M., Sutton T. Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data. Front. Plant Sci. 2018;9:190. doi: 10.3389/fpls.2018.00190. PubMed DOI PMC

Zhang A., Wang H., Beyene Y., Semagn K., Liu Y., Cao S., Cui Z., Ruan Y., Burgueño J., Vicente F.S., et al. Effect of trait heritability, training population size and marker density on genomic prediction accuracy estimation in 22 bi-parental tropical maize populations. Front. Plant Sci. 2017;8:8. doi: 10.3389/fpls.2017.01916. PubMed DOI PMC

Zhang X., Pérez-Rodríguez P., Burgueño J., Olsen M., Buckler E., Atlin G., Prasanna B.M., Vargas M., Vicente F.M.S., Crossa J. Rapid cycling genomic selection in a multiparental tropical maize population. G3 Genes Genomes Genet. 2017;7:2315–2326. doi: 10.1534/g3.117.043141. PubMed DOI PMC

Čermák T., Baltes N.J., Cegan R., Zhang Y., Voytas D.F. High-frequency, precise modification of the tomato genome. Genome Biol. 2015;16:232. doi: 10.1186/s13059-015-0796-9. PubMed DOI PMC

Li J.-F., Norville J.E., Aach J., McCormack M., Zhang D., Bush J., Church G.M., Sheen J. Multiplex and homologous recombination–mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 2013;31:688–691. doi: 10.1038/nbt.2654. PubMed DOI PMC

Ito Y., Nishizawa A., Endo M., Mikami M., Toki S. CRISPR/Cas9-mediated mutagenesis of the RIN locus that regulates tomato fruit ripening. Biochem. Biophys. Res. Commun. 2015;467:76–82. doi: 10.1016/j.bbrc.2015.09.117. PubMed DOI

Feng Z., Mao Y., Xu N., Zhang B., Wei P., Yang N.-L., Wang Z., Zhang Z., Zheng R., Yang L., et al. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2014;111:4632–4637. doi: 10.1073/pnas.1400822111. PubMed DOI PMC

Du H., Zeng X., Zhao M., Cui X., Wang Q., Yang H., Cheng H., Yu D. Efficient targeted mutagenesis in soybean by TALENs and CRISPR/Cas9. J. Biotechnol. 2016;217:90–97. doi: 10.1016/j.jbiotec.2015.11.005. PubMed DOI

Sun Y., Zhang X., Wu C., He Y., Ma Y., Hou H., Guo X., Du W., Zhao Y., Xia L. Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol. Plant. 2016;9:628–631. doi: 10.1016/j.molp.2016.01.001. PubMed DOI

Ma X., Zhang Q., Zhu Q., Liu W., Chen Y., Qiu R., Wang B., Yang Z., Li H., Lin Y., et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant. 2015;8:1274–1284. doi: 10.1016/j.molp.2015.04.007. PubMed DOI

Shi J., Gao H., Wang H., Lafitte H.R., Archibald R.L., Yang M., Hakimi S.M., Mo H., Habben J.E. ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol. J. 2016;15:207–216. doi: 10.1111/pbi.12603. PubMed DOI PMC

Wang L., Chen L., Li R., Zhao R., Yang M., Sheng J., Shen L. Reduced drought tolerance by CRISPR/Cas9-mediated SlMAPK3 mutagenesis in tomato plants. J. Agric. Food Chem. 2017;65:8674–8682. doi: 10.1021/acs.jafc.7b02745. PubMed DOI

Li R., Liu C., Zhao R., Wang L., Chen L., Yu W., Zhang S., Sheng J., Shen L. CRISPR/Cas9-mediated SlNPR1 mutagenesis reduces tomato plant drought tolerance. BMC Plant Biol. 2019;19:38. doi: 10.1186/s12870-018-1627-4. PubMed DOI PMC

Osakabe Y., Watanabe T., Sugano S.S., Ueta R., Ishihara R., Shinozaki K., Osakabe K. Optimization of CRISPR/Cas9 genome editing to modify abiotic stress responses in plants. Sci. Rep. 2016;6:26685. doi: 10.1038/srep26685. PubMed DOI PMC

Zhang H., Zhang J., Wei P., Zhang B., Gou F., Feng Z., Mao Y., Yang L., Zhang H., Xu N., et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol. J. 2014;12:797–807. doi: 10.1111/pbi.12200. PubMed DOI

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