Abstract
Soybean is a temperate photosensitive crop but has adapted to sub-tropical and tropical countries of lower latitudes also. Photoperiodic and maturity genes confer latitudinal adaptation in this crop. Genotyping of accessions of higher latitudes have shown the role of photoinsensitivity, conferred by recessive photoperiodic alleles (e1/e2/e3/e4), in adaptation of the crop to high latitudes but information is not available for lower latitudinal countries like India. We genotyped and calculated the photosensitivity of 101 cultivated Indian soybean varieties and found that majority of the varieties (86) were photosensitive and had the dominant alleles at these loci. Four genotypic classes (e1-as/E2/E3/E4, E1/e2/e3/E4, E1/e2/E3/E4 and E1/E2/e3/E4) were observed for varieties with recessive alleles. Photoinsensitive alleles at E1 and E2 loci significantly reduced the days to flower, maturity and photosensitivity percentage. Adaptive role of photoperiodic alleles was inferred from breeder seed requirement of these varieties for 35 years. Although the photosensitive class contributed 81% to the total seed requirement the weighted mean contribution of this class (380 Q/year) was far less than that of photoinsensitive class (648 Q/year). Photoinsensitivity is essential for perpetuation of crop in higher latitudes. Present report highlights the novel role of photoinsensitive alleles in adaptation of soybean to rainfed, short growing and sub-tropical conditions of lower latitudes by conferring earliness.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agarwal DK, Husain SM, Ramteke R, Bhatia VK, Srivastava SK (2010) Soybean varieties of India. Directorate of Soybean Research, Indore
Anonymous: Annual Report 2018–2019. Indian Institute of Soybean Research, Indore
Bernard RL (1971) Two major genes for time of flowering and in soybeans. Crop Sci 11:242–244. https://doi.org/10.2135/cropsci0011183X001100020022x
Bhatia VS, Yadav S, Rashmi A, Lakshami N, Guruprasad KN (2003) Assessment of photoperiod sensitivity for flowering in Indian soybean varieties. Ind J Plant Physiol 8:81–84
Bonato ER, Vello NA (1999) E6 a dominant gene conditioning early flowering and maturity in soybeans. Genet Mol Biol 22:229–232. https://doi.org/10.1590/S1415-47571999000200016
Buzzell RI (1971) Inheritance of a soybean flowering response to fluorescent day length conditions. Can J Genet Cytol 13:703–707. https://doi.org/10.1139/g71-100
Buzzell RI, Voldeng HD (1980) Inheritance of insensitivity to long day length. Soybean Genet Newsl 7:26–29. https://doi.org/10.1093/jhered/esp113
Carpentieri-PípoloV ALA, Kiihl RAS (2002) Inheritance of a long juvenile period under short-day conditions in soybean. Genet Mol Biol 25:463–469. https://doi.org/10.1590/S1415-47572002000400016
Carpentieri-PípoloV ALA, Kiihl RAS, Rosolem CA (2000) Inheritance of long juvenile period under short day conditions for the BR80–6778 soybean (Glycine max (L.) Merrill) line. Euphytica 112:203–209. https://doi.org/10.1023/A:1003927817278
Cober ER, Voldeng HD (2001) A new soybean and photoperiod-sensitivity locus linked to E1 and T. Crop Sci 41:698–701. https://doi.org/10.2135/cropsci2001.413698x
Cober ER, Tanner JW, Voldeng HD (1996) Genetic control of photoperiod response in early-maturing near-isogenic soybean lines. Crop Sci 36:601–605
Cober ER, Molnar SJ, Charette M, Voldeng HD (2010) A new locus for early in soybean. Crop Sci 50:524–527. https://doi.org/10.2135/cropsci2009.04.0174
Curtis DF, Tanner JW, Luzzi BM, Hume DJ (2000) Agronomic and phenological differences of soybean isolines differing in maturity and growth habit. Crop Sci 40:1624–1629
Destro D, Carpentieri-Pípolo V, Kiihl RAS, Almeida LA (2001) Photoperiodism and genetic control of the long juvenile period in soybean: a review. Crop Breed Appl Biotechnol 1:72–92. https://doi.org/10.13082/1984-7033.v01n01a10
Dos Santos JVM, Valliyodan B, Joshi T, Khan SM, Liu Y, Wang J, Vuong TD, de Oliveira MF, Marcelino-Guimarães FC, Xu D (2016) Evaluation of genetic variation among Brazilian soybean cultivars through genome resequencing. BMC Genom 17:1. https://doi.org/10.1186/s12864-016-3046-y
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Dupare B, Billore SD, Joshi O, Husain SM (2008) Origin, domestication, introduction, and success of soybean in India. Asian Agri-Hist 12:179–195
Ellis RH, Asumadu H, Qi A, Summerfield RJ (2000) Effects of photoperiod and maturity genes on plant growth, partitioning, radiation use efficiency, and yield in soyabean [Glycine max (L.) Merrill] ‘Clark.’ Ann Bot 85(3):335–343. https://doi.org/10.1006/anbo.1999.1072
Fehr WR (1987) Breeding methods for cultivar development. In: Wilcox JR (ed) Soybeans: improvement, production, and uses, 2nd edn. ASA, CSSA and SSSA, Madison, pp 249–293
Fehr WR, Caviness CE (1977) Stages of soybean development. Spec Rep 87. https://lib.dr.iastate.edu/specialreports/87
Fukuda Y (1933) Cytogenetical studies on the wild and cultivated Manchurian soybeans (Glycine L.). Jpn J Bot 6:489–506
Garner WW, Allard HA (1923) Further studies in photoperiodism, the response of the plant to relative length of day and night. Agric Res 23:871–920
Gupta S, Bhatia VS, Kumawat G, Thakur D, Singh G, Tripathi R, Satpute G, Devdas R, Husain SM, Chand S (2017) Genetic analysis for deciphering the status and role of photoperiodic and genes in major Indian soybean cultivar. J Gen 1:147–154. https://doi.org/10.1007/s12041-016-0730-2
Gupta S, Kumawat G, Yadav S et al (2021) Identification and characterization of a novel long juvenile resource AGS 25. Genet Resour Crop Evol. https://doi.org/10.1007/s10722-020-01055-7
Hartwig EE (1973) Varietal development. In: Caldwell BE (ed) Soybeans: improvement, production and uses. ASA, Madison, pp 187–207
Hartwig EE, Edwards C (1987) USDA southern soybean germplasm report. Soybean Genet Newslett 14:14–20
Hymowitz T, Newell CA (1981) Taxonomy of genus Glycine, domestication and uses of soybeans. Econ Bot 35:272–288
Islam MR, Fujita D, Watanabe S, Zheng SH (2018) Variation in photosensitivity of flowering in the world soybean mini-core collections (GmWMC). Plant Prod Sci. https://doi.org/10.1080/1343943X.2018.1561197
Jiang B, Nan H, Gao Y, Tang L, Yue Y, Lu S et al (2014) Allelic combinations of soybean maturity loci E1, E2, E3 and E4 result in diversity of maturity and adaptation to different latitudes. PLoS ONE 9:e106042. https://doi.org/10.1371/journal.pone.0106042
Kong F, Nan H, Cao D, Li Y, Wu F, Wang J et al (2014) A new dominant gene E9 conditions early flowering and maturity in soybean. Crop Sci 54:2529–2535. https://doi.org/10.2135/cropsci2014.03.0228
Kumawat G, Maranna S, Gupta S, Tripathi R, Agrawal N et al (2020) Identification of novel genetic sources for agronomic and quality traits in soybean using multi-trait allele specific genic marker assays. J Plant Biochem Biotechnol. https://doi.org/10.1007/s13562-020-00580-x
Lawn RJ, James AT (2011a) Application of physiological understanding in soybean improvement. I. Understanding phenological constraints to adaptation and yield potential. Crop Pasture Sci 62:1–11. https://doi.org/10.1071/CP10289
Lawn RJ, James AT (2011b) Application of physiological understanding in soybean improvement. II. Broadening phenological adaptation across regions and sowing dates. Crop Pasture Sci 62:12–24
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al (2009) The sequence alignment/map format and SAM tools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
McBlain BA, Bernard RL (1987) A new gene affecting the time of flowering and maturity in soybean. J Hered 78:160–162. https://doi.org/10.1093/oxfordjournals.jhered.a110349
Meng L, Huihui L, Zhang L, Wang J (2015) QTL ICI mapping: integrated software genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283. https://doi.org/10.1016/j.cj.2015.01.001
Merry R, Butenhoff K, Campbell BW, Michno JM, Wang D, Orf JH, Lorenz AJ, Stupar RM (2019) Identification and fine-mapping of a soybean quantitative trait locus on chromosome 5 conferring tolerance to iron deficiency chlorosis. Plant Genome 12:190007. https://doi.org/10.3835/plantgenome2019.01.0007
Miladinović J, Ćeran M, Đorđević V, Balešević-Tubić S, Petrović K, Đukić V, Miladinović D (2018) Allelic variation and distribution of the major maturity genes in different soybean collections. Front Plant Sci 9:1286. https://doi.org/10.3389/fpls.2018.01286
Miranda C, Scaboo A, Cober E et al (2020) The effects and interaction of soybean maturity gene alleles controlling flowering time, maturity, and adaptation in tropical environments. BMC Plant Biol 20:65. https://doi.org/10.1186/s12870-020-2276-
Poehlman JM (1987) Breeding soybeans. In: Poehlman JM (ed) Breeding field crops, 3rd edn. Van Nostrand Reinhold, New York, pp 421–450
Ray JD, Hinson K, Mankono JEB, Malo MF (1995) Genetic control of a long-juvenile trait in soybean. Crop Sci 35:1001–1006. https://doi.org/10.2135/cropsci1995.0011183X003500040012x
Saindon G, Voldeng HD, Beversdorf WD, Buzzell RI (1989) Genetic control of long daylength response in soybean. Crop Sci 29:1436–1439
Samanfar B, Molnar SJ, Charette M, Schoenrock A, Dehne F, Golshani A et al (2017) Mapping and identification of a potential candidate gene for a novel maturity locus, E10, in soybean. Appl Genet 130:377–390. https://doi.org/10.1007/s00122-016-2819-7
Tsubokura Y, Matsumura H, Xu M, Liu B, Nakashima H, Anai T, Kong F, Yuan X, Kanamori H, Katayose Y, Takahashi R, Harada K, Abe J (2013) Genetic variation in soybean at the maturity locus E4 is involved in adaptation to long days at high latitudes. Agronomy 3:117–134. https://doi.org/10.3390/agronomy3010117
Tsubokura Y, Watanabe S, Xia Z, Kanamori H, Yamagata H, Kaga A, Katayose Y, Abe J, Ishimoto M, Harada K (2014) Natural variation in the genes responsible for maturity loci E1, E2, E3 and E4 in soybean. Ann Bot (Lond) 113:429–441
Vavilov NI (1951) The origin variation immunity and breeding of cultivated plants (translation by K Star Chester). Chron Bot Ronald Press, NewYork
Wang F, Nan H, Chen L, Fang C, Zhang H, Su T, Li S, Cheng Q, Dong L, Liu B, Kong F, Lu S (2019) A new dominant locus, E11, controls early flowering time and maturity in soybean. Mol Breed 39:70. https://doi.org/10.1007/s11032-019-0978-3
Watanabe S, Hideshima R, Xia Z, Tsubokura Y, Sato S, Nakamoto Y, Yamanaka N, Takahashi R, Ishimoto M, Anai T, Tabata S, Harada K (2009) Map-based cloning of the gene associated with the soybean maturity locus E3. Genetics 182:1251–1262. https://doi.org/10.1534/genetics.108.098772
Watanabe S, Xia Z, Hideshima R, Tsubokura Y, Sato S, Harada K (2011) A map-based cloning strategy employing a residual heterozygous line reveals that the GIGANTEA gene is involved in soybean maturity and flowering. Genetics 188:395–407. https://doi.org/10.1534/genetics.110.125062
Watanabe S, Harada K, Abe J (2012) Genetic and molecular basis of photoperiod responses of flowering in soybean. Breed Sci 61:531–543. https://doi.org/10.1270/jsbbs.61.531
Whigham DK, Minor HC (1978) Agronomic characteristics and environmental stress. In: Norman AG (ed) Soybean physiology, agronomy, and utilization. Academic Press, New York, pp 77–112
Wolfgang G, An YQC (2017) Genetic separation of southern and northern soybean breeding programs in North America and their associated allelic variation at four maturity loci. Mol Breed 37:8. https://doi.org/10.1007/s11032-016-0611-7
Xu M, Xu Z, Liu B, Kong F, Tsubokura Y, Watanabe S, Xia Z, Harada K, Kanazawa A, Yamada T, Abe J (2013) Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean. BMC Plant Biol 13:91. https://doi.org/10.1186/1471-2229-13-91
Zhang LX, Kyei-Boahen S, Zhang J, Zhang MH, Freeland TB, Watson CE Jr et al (2007) Modifications of optimum adaptation zones for soybean maturity groups in the USA. Crop Manag 6:1–11
Acknowledgements
Authors are thankful to Director, ICAR-IISR, Indore for providing all the required facilities for the experiments. Authors are thankful to Department of Biotechnology, Ministry of science and technology for providing research grant.
Author information
Authors and Affiliations
Contributions
SG and GK planned all experiments and coordinated the work; RT performed phenotyping and genotyping for photosensitivity calculation; VSB conceptualized the idea; VN, GKS, SM and MR analyzed data; MK, PK and NA conducted large field trials and compiled seed data, RV, SC recorded data and SC helped in writing of manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tripathi, R., Agrawal, N., Kumawat, G. et al. Novel role of photoinsensitive alleles in adaptation of soybean [Glycine max (L.) Merr.] to rainfed short growing seasons of lower latitudes. Genet Resour Crop Evol 68, 2455–2467 (2021). https://doi.org/10.1007/s10722-021-01142-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10722-021-01142-3