Abstract
Amaranth (Amaranthus spp.) belonging to Amaranthaceae, is known as “the crop of the future” because of its incredible nutritional quality. Amaranthus spp. (> 70) have a huge diversity in terms of their plant morphology, production and nutritional quality; however, these species are not well characterized at molecular level due to unavailability of robust and reproducible molecular markers, which is essential for crop improvement programs. In the present study, 13,051 genome-wide microsatellite motifs were identified and subsequently utilized for marker development using A. hypochondriacus (L.) genome (JPXE01.1). Out of those, 1538 motifs were found with flanking sequences suitable for primer designing. Among designed primers, 225 were utilized for validation of which 119 (52.89%) primers were amplified. Cross-species transferability and evolutionary relatedness among ten species of Amaranthus (A. hypochondriacus, A. caudatus, A. retroflexus, A. cruentus, A. tricolor, A. lividus, A. hybridus, A. viridis, A. edulis, and A. dubius) were also studied using 45 microsatellite motifs. The maximum (86.67%) and minimum (28.89%) cross-species transferability were observed in A. caudatus and A. dubius, respectively, that indicated high variability present across the Amaranthus spp. Total 97 alleles were detected among 10 species of Amaranthus. The averages of major allele frequency, gene diversity, heterozygosity and PIC were 0.733, 0.347, 0.06, and 0.291, respectively. Nei’s genetic dissimilarity coefficients ranged from 0.0625 (between A. tricolor and A. hybridus) to 0.7918 (between A. viridis and A. lividus). The phylogenetic tree grouped ten species into three major clusters. Genome-wide development of microsatellite markers and their transferability revealed relationships among amaranth species which ultimately can be useful for species identification, DNA fingerprinting, and QTLs/gene(s) identification.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
Not applicable.
Code availability
Not applicable.
References
Alegbejo JO (2013) Nutritional value and utilization of Amaranthus (Amaranthus spp.)–a review. Bayero J Pure Appl Sci 6(1):136–143. https://doi.org/10.4314/bajopas.v6i1.27
Alsamman AM, Ibrahim SD, Hamwieh A (2019) KASPspoon: an in vitro and in silico PCR analysis tool for high-throughput SNP genotyping. Bioinformatics 35(17):3187–3190. https://doi.org/10.1093/bioinformatics/btz004
Beier S, Thiel T, Münch T, Scholz U, Mascher M (2017) MISA-web: a web server for microsatellite prediction. Bioinformatics 33(16):2583–2585. https://doi.org/10.1093/bioinformatics/btx198
Bhat A, Satpathy G, Gupta RK (2015) Evaluation of nutraceutical properties of Amaranthus hypochondriacus L. grains and formulation of value added cookies. J Pharmacogn Phytochem 3(5):51–54
Celik I, Gultekin V, Allmer J, Doganlar S, Frary A (2014) Development of genomic simple sequence repeat markers in opium poppy by next-generation sequencing. Mol Breed 34(2):323–334. https://doi.org/10.1007/s11032-014-0036-0
Chandra A, Tiwari KK, Nagaich D, Dubey N, Kumar S, Roy AK (2011) Development and characterization of microsatellite markers from tropical forage Stylosanthes species and analysis of genetic variability and cross-species transferability. Genome 54(12):1016–1028. https://doi.org/10.1139/g11-064
Chaudhari BA, Patel MP, Dharajiya DT, Tiwari KK (2019) Assessment of genetic diversity in castor (Ricinus communis L.) using microsatellite markers. Biosci Biotechnol Res Asia 16(1):61–69. https://doi.org/10.13005/bbra/2721
Chen X, Temnykh S, Xu Y, Cho YG, McCouch SR (1997) Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theor Appl Genet 95(4):553–567
Clouse JW, Adhikary D, Page JT, Ramaraj T, Deyholos MK, Udall JA, Fairbanks DJ, Jellen EN, Maughan PJ (2016) The amaranth genome: genome, transcriptome, and physical map assembly. The Plant Genome 9(1):1–14. https://doi.org/10.3835/plantgenome2015.07.0062
Coelho LM, Silva PM, Martins JT, Pinheiro AC, Vicente AA (2018) Emerging opportunities in exploring the nutritional/functional value of amaranth. Food Funct 9(11):5499–5512. https://doi.org/10.1039/C8FO01422A
Das S (2016) Amaranthus: A promising crop of future. Springer, Singapore, p 208. https://doi.org/10.1007/978-981-10-1469-7
Dharajiya DT, Shah A, Galvadiya BP, Patel MP, Srivastava R, Pagi NK, Solanki SD, Parida SK, Tiwari KK (2020) Genome-wide microsatellite markers in castor (Ricinus communis L.): Identification, development, characterization, and transferability in Euphorbiaceae. Ind Crops Prod 151:112461. https://doi.org/10.1016/j.indcrop.2020.112461
Dharajiya DT, Singh AK, Tiwari KK, Prajapati NN (2021) Genetic diversity in amaranth and its close relatives. In: Adhikary D, Deyholos MK, Délano-Frier JP (eds) The amaranth genome. Compendium of plant genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-72365-1_6
Doyle J (1991) DNA protocols for plants. Molecular techniques in taxonomy. Springer, Berlin, pp 283–293
Dua RP, Raiger HL, Phogat BS, Sharma SK (2009) Underutilized crops: improved varieties and cultivation practices. NBPGR, New Delhi, p 66
Gelotar MJ, Dharajiya DT, Solanki SD, Prajapati NN, Tiwari KK (2019) Genetic diversity analysis and molecular characterization of grain amaranth genotypes using inter simple sequence repeat (ISSR) markers. Bull Natl Res Cent 43(1):103. https://doi.org/10.1186/s42269-019-0146-2
He Q, Park YJ (2013) Evaluation of genetic structure of amaranth accessions from the United States. Weed Turf Sci 2(3):230–235. https://doi.org/10.5660/WTS.2013.2.3.230
Kaldate R, Rana M, Sharma V, Hirakawa H, Kumar R, Singh G, Chahota RK, Isobe SN, Sharma TR (2017) Development of genome-wide SSR markers in horsegram and their use for genetic diversity and cross-transferability analysis. Mol Breed 37(8):103. https://doi.org/10.1007/s11032-017-0701-1
Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177(3):309–334. https://doi.org/10.1007/s10681-010-0286-9
Khaing AA, Moe KT, Chung JW, Baek HJ, Park YJ (2013) Genetic diversity and population structure of the selected core set in Amaranthus using SSR markers. Plant Breed 132(2):165–173. https://doi.org/10.1111/pbr.12027
Kumari R, Wankhede DP, Bajpai A, Maurya A, Prasad K, Gautam D, Rangan P, Latha M, John KJ, Bhat KV, Gaikwad AB (2019) Genome wide identification and characterization of microsatellite markers in black pepper (Piper nigrum): a valuable resource for boosting genomics applications. PLoS ONE 14(12):e0226002. https://doi.org/10.1371/journal.pone.0226002
Lee RM, Thimmapuram J, Thinglum KA, Gong G, Hernandez AG, Wright CL, Kim RW, Mikel MA, Tranel PJ (2009) Sampling the waterhemp (Amaranthus tuberculatus) genome using pyrosequencing technology. Weed Sci 57(5):463–469. https://doi.org/10.1614/WS-09-021.1
Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11(12):2453–2465
Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21(9):2128–2129. https://doi.org/10.1093/bioinformatics/bti282
Mallory MA, Hall RV, McNabb AR, Pratt DB, Jellen EN, Maughan PJ (2008) Development and characterization of microsatellite markers for the grain amaranths. Crop Sci 48(3):1098–1106. https://doi.org/10.2135/cropsci2007.08.0457
Martinez-Lopez A, Millan-Linares MC, Rodriguez-Martin NM, Millan F, Montserrat Paz S (2020) Nutraceutical value of kiwicha (Amaranthus caudatus L.). J Funct Foods 65:103735. https://doi.org/10.1016/j.jff.2019.103735
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19(2):153–170
Nguyen DC, Tran DS, Tran T, Ohsawa R, Yoshioka Y (2019) Genetic diversity of leafy amaranth (Amaranthus tricolor L.) resources in Vietnam. Breed Sci 69(4):640–650. https://doi.org/10.1270/jsbbs.19050
Oo WH, Park YJ (2013) Analysis of the genetic diversity and population structure of amaranth accessions from South America using 14 SSR markers. Korean J Crop Sci 58(4):336–346. https://doi.org/10.7740/kjcs.2013.58.4.336
Pagi N, Prajapati N, Pachchigar K, Dharajiya D, Solanki SD, Soni N, Patel P (2017) GGE biplot analysis for yield performance of grain amaranth genotypes across different environments in western India. J Exp Biol Agric Sci 5(3):368–376. https://doi.org/10.18006/2017.5(3).368.376
Pandey G, Misra G, Kumari K, Gupta S, Parida SK, Chattopadhyay D, Prasad M (2013) Genome-wide development and use of microsatellite markers for large-scale genotyping applications in foxtail millet [Setaria italica (L.)]. DNA Res 20(2):197–207. https://doi.org/10.1093/dnares/dst002
Parita B, Kumar SN, Darshan D, Karen P (2018) Elucidation of genetic diversity among ashwagandha [Withania somnifera (L.) Dunal] genotypes using EST-SSR markers. Res J Biotechnol 13(10):52–59
Peter K, Gandhi P (2017) Rediscovering the therapeutic potential of Amaranthus species: a review. Egypt J Basic Appl Sci 4(3):196–205. https://doi.org/10.1016/j.ejbas.2017.05.001
Singh D, Singh CK, Tribuvan KU, Tyagi P, Taunk J, Tomar RSS, Kumari S, Tripathi K, Kumar A, Gaikwad K, Yadav RK (2020) Development, characterization, and cross species/genera transferability of novel EST-SSR markers in lentil, with their molecular applications. Plant Mol Biol Rep 38(1):114–129. https://doi.org/10.1007/s11105-019-01184-z
Sonah H, Deshmukh RK, Sharma A, Singh VP, Gupta DK, Gacche RN, Rana JC, Singh NK, Sharma TR (2011) Genome-wide distribution and organization of microsatellites in plants: an insight into marker development in Brachypodium. PLoS ONE 6(6):e21298. https://doi.org/10.1371/journal.pone.0021298
Stetter MG, Schmid KJ (2017) Analysis of phylogenetic relationships and genome size evolution of the Amaranthus genus using GBS indicates the ancestors of an ancient crop. Mol Phylogenet Evol 109:80–92. https://doi.org/10.1016/j.ympev.2016.12.029
Stetter MG, Müller T, Schmid KJ (2017) Genomic and phenotypic evidence for an incomplete domestication of South American grain amaranth (Amaranthus caudatus). Mol Ecol 26(3):871–886. https://doi.org/10.1111/mec.13974
Sunil M, Hariharan AK, Nayak S, Gupta S, Nambisan SR, Gupta RP, Panda B, Choudhary B, Srinivasan S (2014) The draft genome and transcriptome of Amaranthus hypochondriacus: a C4 dicot producing high-lysine edible pseudo-cereal. DNA Res 21(6):585–602. https://doi.org/10.1093/dnares/dsu021
Suresh S, Chung JW, Cho GT, Sung JS, Park JH, Gwag JG, Baek HJ (2014) Analysis of molecular genetic diversity and population structure in Amaranthus germplasm using SSR markers. Plant Biosyst 148(4):635–644. https://doi.org/10.1080/11263504.2013.788095
Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106(3):411–422. https://doi.org/10.1007/s00122-002-1031-0
Tiwari KK, Pattnaik S, Singh A, Sandhu M, Mithra SA, Abdin MZ, Singh AK, Mohapatra T (2014) Allelic variation in the microsatellite marker locus RM6100 linked to fertility restoration of WA based male sterility in rice. Indian J Genet 74(4):409–413. https://doi.org/10.5958/0975-6906.2014.00863.3
Udupa S, Baum M (2001) High mutation rate and mutational bias at (TAA)n microsatellite loci in chickpea (Cicer arietinum L.). Mol Genet Genom 265(6):1097–1103. https://doi.org/10.1007/s004380100508
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):e115–e115. https://doi.org/10.1093/nar/gks596
Viljoen E, Odeny DA, Coetzee MP, Berger DK, Rees DJ (2018) Application of chloroplast phylogenomics to resolve species relationships within the plant genus Amaranthus. J Mol Evol 86(3):216–239. https://doi.org/10.1007/s00239-018-9837-9
Wang XQ, Park YJ (2013) Comparison of genetic diversity among amaranth accessions from South and Southeast Asia using SSR markers. Korean J Med Crop Sci 21(3):220–228. https://doi.org/10.7783/KJMCS.2013.21.3.220
Wang MX, Zhang HL, Zhang DL, Qi YW, Fan ZL, Li DY, Pan DJ, Cao YS, Qiu ZE, Yu P, Yang QW, Wang XK, Li ZC (2008) Genetic structure of Oryza rufipogon Griff. China Heredity 101(6):527–535. https://doi.org/10.1038/hdy.2008.61
Wang X, Yang S, Chen Y, Zhang S, Zhao Q, Li M, Gao Y, Yang L, Bennetzen JL (2018) Comparative genome-wide characterization leading to simple sequence repeat marker development for Nicotiana. BMC Genomics 19(1):500. https://doi.org/10.1186/s12864-018-4878-4
Xiao Y, Xia W, Ma J, Mason AS, Fan H, Shi P, Lei X, Ma Z, Peng M (2016) Genome-wide identification and transferability of microsatellite markers between Palmae species. Front Plant Sci 7:1578. https://doi.org/10.3389/fpls.2016.01578
Acknowledgements
The authors are thankful to the authorities of C. P. College of Agriculture, SDAU, Sardarkrushinagar, Gujarat, India, to avail facilities to conduct the research. The authors are also thankful to the Gujarat State Biotechnology Mission (GSBTM), Department of Science and Technology (DST), Government of Gujarat, Gandhinagar, India for the financial assistance.
Funding
The funding was provided by Gujarat State Biotechnology Mission (GSBTM), Department of Science and Technology (DST), Government of Gujarat, Gandhinagar, Gujarat, India (Grant no. 1362).
Author information
Authors and Affiliations
Contributions
Conceptualization: KKT, NNP, MPP; Methodology: KKT, NNP, MPP; Formal analysis and investigation: NJT, DTD, HLB, PPB, BPG; Writing—original draft preparation: KKT, DTD; Writing—review and editing: KKT, DTD, NNP, MPP, SDS; Funding acquisition: KKT; Resources: NNP, MPP, SDS; Supervision: KKT, NNP, MPP, SDS.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest.
Consent for publication
Not applicable.
Ethics approval
Not applicable.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tiwari, K.K., Thakkar, N.J., Dharajiya, D.T. et al. Genome-wide microsatellites in amaranth: development, characterization, and cross-species transferability. 3 Biotech 11, 395 (2021). https://doi.org/10.1007/s13205-021-02930-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-021-02930-5