Abstract
Common bean is a nutrient‐dense legume crop serving as a source of food for millions of people. Characterization of unexplored common bean germplasm to unlock the phenotypic and genetic variations is still needed to explore the breeding potential of this crop. The current study aimed to dissect the genetic basis having association for days to flowering (DF). A total of 188 common bean accessions collected from 19 provinces of Turkey were used as plant material under five environments and two locations. Analysis of variance (ANOVA) revealed that genotypes and genotype by environment interaction have significant effects on DF. A total of 10 most stable accessions were evaluated from stability analysis. Overall maximum (75) and minimum (54) DF were observed for Hakkari-51 and Mus-46 accessions, respectively. The implemented constellation plot divided studied germplasm according to their DF and growth habit. A total of 7900 DArTseq markers were used for association analysis. Mixed linear model using the Q + K Model resulted a total of 18 DArTseq markers from five environments. DArT-8668385 marker identified in Bolu during 2016 was also associated with DF in Sivas during 2017. Combined data of five years resulted a total of four markers (DArT-22346534, DArT-3369768, DArT-3374613, and DArT-3370801) having significant association ( p < 0.01 ) for DF. DArT-22346534 present on Pv 08 accounted a maximum of 9.89% variation to the studied trait. A total of four putative candidate genes were predicted from sequences reflecting homology to identified four DArTseq markers. We envisage that exploitation of identified DArTseq markers will hopefully beneficial for the development of new common bean varieties having better adaptation ability to changing climatic conditions.
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References
Alexandratos N, Bruinsma J (2012) World Agriculture towards 2030/2050. The 2012 Revision. Global Perspective Studies Team. ESA Working Paper No. 12–03. Rome, Italy FAO, Food and Agriculture Organization of the United Nations
Ali F, Nadeem MA, Barut M, Habyarimana E, Chaudhary HJ, Khalil IH, Alsaleh A, Hatipoğlu R, Karaköy T, Kurt C, Aasim M (2020) Genetic diversity, population structure and marker-trait association for 100-seed weight in international safflower panel using SilicoDArT marker information. Plants 9:652
Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639
Arystanbekkyzy M, Nadeem MA, Aktas H, Yeken MZ, Zencirci N, Nawaz MA, Ali F, Haider MS, Tunc K, Chung G, Baloch FS (2019) Phylogenetic and taxonomic relationship of turkish wild and cultivated emmer (triticum turgidum ssp. dicoccoides) revealed by iPBSretrotransposons markers. Int J Agric Biol 21:155–163
Ates D, Asciogul TK, Nemli S, Erdogmus S, Esiyok D, Tanyolac MB (2018) Association mapping of days to flowering in common bean (Phaseolus vulgaris L.) revealed by DArT markers. Mol Breed 38:113
Aydin MF, Baloch FS (2019) Exploring the genetic diversity and population structure of Turkish common bean germplasm by the iPBS-retrotransposons markers. Legume Res Int J 42:18–24
Baloch FS, Alsaleh A, Shahid MQ, Çiftçi V, E. Sáenz de Miera L, Aasim M, Nadeem MA, Aktaş H, Özkan H, Hatipoğlu R (2017) A whole genome DArTseq and SNP analysis for genetic diversity assessment in durum wheat from central fertile crescent. PloS one 12: e0167821
Bhakta MS, Gezan SA, Michelangeli JA, Carvalho M, Zhang L, Jones JW, Boote KJ, Correll MJ, Beaver J, Osorno JM, Colbert R (2017) A predictive model for time-to-flowering in the common bean based on QTL and environmental variables. G3: genes. Genomes Genet 7:3901–3912
Bitocchi E, Nanni L, Bellucci E, Rossi M, Giardini A, Zeuli PS, Logozzo G, Stougaard J, McClean P, Attene G, Papa R (2012) Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proc Natl Acad Sci 109:E788–E796
Bitocchi E, Rau D, Benazzo A, Bellucci E, Goretti D, Biagetti E, Panziera A, Laido G, Rodriguez M, Gioia T, Attene G (2017) High level of nonsynonymous changes in common bean suggests that selection under domestication increased functional diversity at target traits. Front Plant Sci 7:2005. https://doi.org/10.3389/fpls.2016.02005
Bozoglu H, Sozen O (2011) A sample for biodiversity in Turkey: Common bean (Phaseolus vulgaris L.) landraces from Artvin. Afr J Biotechnol 10:13789–13796
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Ceylan A, Öcal N, Akbulut M (2014) Genetic diversity among the Turkish common bean cultivars (Phaseolus vulgaris L.) as assessed by SRAP, POGP and cpSSR markers. Biochem Syst Ecol 54:219–229
Cockram J, Jones H, Leigh FJ, O’Sullivan D, Powell W, Laurie DA, Greenland AJ (2007) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J Exp Bot 58:1231–1244
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510
De Mendiburu F, Simon R (2015) Agricolae-Ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ PrePrints e1748
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Ebdon JS, Gauch HG Jr (2002) Additive main effect and multiplicative interaction analysis of national turfgrass performance trials: I. Interpretation of genotype × environment interaction. Crop Sci 42:489–496
Eberhart ST, Russell WA (1966) Stability parameters for comparing varieties 1. Crop Sci 1966(6):36–40
Finlay KW, Wilkinson GN (1963) The analysis of adaptation in a plant-breeding programme. Aust J Agric Res 14:742–754
Fivawo NC, Nchimbi-Msolla S (2012) The diversity of common bean landraces in Tanzania Phase II multi-location trial. Tanz J Nat Appl Sci 3:500–516
Flores F, Moreno MT, Cubero JI (1998) A comparison of univariate and multivariate methods to analyze G × E interaction. Field Crop Res 56:271–286
Food and Agriculture Organization (2021) FAO Statistical Yearbook. 2021. Available online: http://www.fao.org/docrep/017/i3138e/i3138e. Accessed 17 June 2021
Fritsche-Neto R, Souza TL, Pereira HS, Faria LC, Melo LC, Novaes E, Brum IJ, Jannink JL (2019) Association mapping in common bean revealed regions associated with Anthracnose and Angular Leaf Spot resistance. Sci Agr 76:321–327
Fróna D, Szenderák J, Harangi-Rákos M (2019) The challenge of feeding the world. Sustainability 11:5816
Gauch HG, Moran DR (2019) AMMISOFT for AMMI analysis with best practices. BioRxiv https://doi.org/10.1101/538454
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research, 2nd edn. John Wiley & Sons Inc, New York, USA
Hepworth SR, Klenz JE, Haughn GW (2006) UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta 223:769–778
Hoyos-Villegas V, Song Q, Kelly JD (2017) Genome-wide association analysis for drought tolerance and associated traits in common bean. Plant Genome 10:1–7
Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483
Kamfwa K, Cichy KA, Kelly JD (2015a) Identification of quantitative trait loci for symbiotic nitrogen fixation in common bean. Theor Appl Genet 132:1375–1387
Kamfwa K, Cichy KA, Kelly JD (2015b) Genome-wide association study of agronomic traits in common bean. Plant Genome 8:2014–2109
Khaidizar MI, Haliloglu K, Elkoca E, Aydin M, Kantar F (2012) Genetic diversity of common bean (Phaseolus vulgaris L.) landraces grown in northeast Anatolia of Turkey assessed with simple sequence repeat markers. Turk J Field Crops 17:145–150
Khush GS, Lee S, Cho JI, Jeon JS (2012) Biofortification of crops for reducing malnutrition. Plant Biotechnol Rep 6:195–202
Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Ann Rev Cell Dev 25:277–299
Kobayashi-Uehara A, Shimosaka E, Handa H (2001) Cloning and expression analyses of cDNA encoding an ADP-ribosylation factor from wheat: tissue-specific expression of wheat ARF. Plant Sci 160:535–542
Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:1–9
Langer SM, Longin CF, Würschum T (2014) Flowering time control in European winter wheat. Front Plant Sci 5:537
MendesMP BFBS, Ramalho MAP, Abreu ÂFB, Furtini IV (2008) Genetic control of the number of days to flowering in common bean. Crop Breed Appl Biotechnol 8:279–282
Moghaddam SM, Mamidi S, Osorno JM, Lee R, Brick M, Kelly J, Miklas P, Urrea C, Song Q, Cregan P, Grimwood J (2016) Genome-wide association study identifies candidate loci underlying agronomic traits in a Middle American diversity panel of common bean. Plant Genome 9:1–21
Montgomery BL, Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7:357–366
Mühleisen J, Piepho HP, Maurer HP, Longin CF, Reif JC (2014) Yield stability of hybrids versus lines in wheat, barley, and triticale. Theor Appl Genet 127:309–316
Mukeshimana G, Butare L, Cregan PB, Blair MW, Kelly JD (2014) Quantitative trait loci associated with drought tolerance in common bean. Crop Sci 54:923–938
Muthamilarasan M, Mangu VR, Zandkarimi H, Prasad M, Baisakh N (2016) Structure, organization and evolution of ADP-ribosylation factors in rice and foxtail millet and their expression in rice. Sci Rep 6:1–3
Mvile B (2015) Genotype x environment interaction of common bean (Phaseolus vulgaris L.) genotypes on reaction to four bean diseases. Ph.D dissertation, Sokoine University of Agriculture Tanzania
Nadeem MA, Nawaz MA, Shahid MQ, Doğan Y, Comertpay G, Yıldız M, Hatipoğlu R, Ahmad F, Alsaleh A, Labhane N, Özkan H (2018a) DNA molecular markers in plant breeding: current status and recent advancements in genomic selection and genome editing. Biotechnol Biotechnol Equip 32:261–285
Nadeem MA, Habyarimana E, Çiftçi V, Nawaz MA, Karaköy T, Comertpay G, Shahid MQ, Hatipoğlu R, Yeken MZ, Ali F, Ercişli S (2018) Characterization of genetic diversity in Turkish common bean gene pool using phenotypic and whole-genome DArTseq-generated silicoDArT marker information. PloS one 13:e0205363
Nadeem MA, Gündoğdu M, Ercişli S, Karaköy T, Saracoğlu O, Habyarimana E, Lin X, Hatipoğlu R, Nawaz MA, Sameeullah M, Ahmad F (2020a) Uncovering phenotypic diversity and DArTseq marker loci associated with antioxidant activity in common bean. Genes 11:36
Nadeem MA, Karaköy T, Yeken MZ, Habyarimana E, Hatipoğlu R, Çiftçi V, Nawaz MA, Sönmez F, Shahid MQ, Yang SH, Chung G (2020b) Phenotypic characterization of 183 Turkish common bean accessions for agronomic, trading, and consumer-preferred plant characteristics for breeding purposes. Agronomy 10:272
Nadeem MA, Yeken MZ, Shahid MQ, Habyarimana E, Yılmaz H, Alsaleh A, Hatipoğlu R, Çilesiz Y, Khawar KM, Ludidi N, Ercişli S, Aasim M, Karaköy T, Baloch FS (2021) Common bean as a potential crop for future food security: an overview of past, current and future contributions in genomics, transcriptomics, transgenics and proteomics. Biotechnol Biotechnol Equip 35:758–786
Ozturk I, Kara M, Yildiz C, Ercisli S (2009) Physico-mechanical seed properties of the common Turkish bean (Phaseolus vulgaris) cultivars ‘Hinis’ and ‘Ispir.’ New Zeal J Crop Hort 37:41–50
Pérez-Vega E, Pañeda A, Rodríguez-Suárez C, Campa A, Giraldez R, Ferreira JJ (2010) Mapping of QTLs for morpho-agronomic and seed quality traits in a RIL population of common bean (Phaseolus vulgaris L.). Theor Appl Genet 120:1367–1380
Petry N, Boy E, Wirth JP, Hurrell RF (2015) The potential of the common bean (Phaseolus vulgaris) as a vehicle for iron biofortification. Nutrients 7:1144–1173
Pikaard CS, Haag JR, Ream T, Wierzbicki AT (2008) Roles of RNA polymerase IV in gene silencing. Trends Plant Sci 13:390–397
Pour-Aboughadareh A, Yousefian M, Moradkhani H, Poczai P, Siddique KH (2019) STABILITYSOFT: a new online program to calculate parametric and non-parametric stability statistics for crop traits. Appl Plant Sci 7:e01211
Raggi L, Caproni L, Carboni A, Negri V (2019) Genome-wide association study reveals candidate genes for flowering time variation in common bean (Phaseolus vulgaris L.). Front Plant Sci 10:962
Rathore A, Parsad R, Gupta VK (2004) Computer aided construction and analysis of augmented designs. J Indian Soc Agric Stat 57:320–344
Rebello CJ, Greenway FL, Finley JW (2014) Whole grains and pulses: a comparison of the nutritional and health benefits. J Agric Food Chem 62:7029–7049
Sasaki E, Frommlet F, Nordborg M (2017) The genetic architecture of the network underlying flowering time variation in Arabidopsis thaliana. BioRxiv 1:175430
Shukla GK (1972) Some statistical aspects of partitioning genotype environmental components of variability. Heredity 29:237–245
Singh NB, Ariyanayagam RP, Gupta SC, Rao AN (1995) Relationship of plant height, days to flowering and maturity to grain yield in short-duration determinate pigeonpea. Indian J Genet Pl Br 55:1–5
Tafesse EG, Gali KK, Lachagari VB, Bueckert R, Warkentin TD (2020) Genome-wide association mapping for heat stress responsive traits in field pea. Int J Mol Sci 21:2043
Turner SD (2014) qqman: an R package for visualizing GWAS results using QQ and manhattan plots. Biorxiv 005165
Vaezi B, Pour-Aboughadareh A, Mehraban A, Hossein-Pour T, Mohammadi R, Armion M, Dorri M (2018) The use of parametric and non-parametric measures for selecting stable and adapted barley lines. Arch Agron Soil Sci 64:597–611
Wallace DH, Baudoin JP, Beaver J, Coyne DP, Halseth DE, Masaya PN, Munger HM, Myers JR, Silbernagel M, Yourstone KS, Zobel RW (1993) Improving efficiency of breeding for higher crop yield. Theor Appl Genet 86:27–40
Wang H, Huang J, Lai Z, Xue Y (2002) F-box proteins in flowering plants. Chin Sci Bull 47:1497–1501
Wang X, Feng S, Nakayama N, Crosby WL, Irish V, Deng XW, Wei N (2003) The COP9 signalosome interacts with SCFUFO and participates in Arabidopsis flower development. Plant Cell 15:1071–1082
Wang Y, Liu K, Liao H, Zhuang C, Ma H, Yan X (2008) The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biol 10:548–562
Wang Q, Tang J, Han B, Huang X (2020) Advances in genome-wide association studies of complex traits in rice. Theor Appl Genet 133:1415–1425
Wricke G (1962) Übereine Methode zur Erfassung der ökologischen Streubreite in Feldversuchen. Zeitschrift Für Pflanzenzüchtung 47:92–96
Zhang J, Song Q, Cregan PB, Nelson RL, Wang X, Wu J, Jiang GL (2015) Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm. BMC Genomics 16:217
Zia MA, Demirel U, Nadeem MA, Caliskan ME (2020) Genome-wide association study identifies various loci underlying agronomic and morphological traits in diversified potato panel. Physiol Mol Biol Plants 26:1003–1020
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The authors express their gratitude to Scientific and Technological Research Council of Turkey (TÜBİTAK) to FSB for providing research grants for this study under the project no: TOVAG-2015O630.
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Nadeem, M.A., Habyarimana, E., Karaköy, T. et al. Genetic dissection of days to flowering via genome-wide association studies in Turkish common bean germplasm. Physiol Mol Biol Plants 27, 1609–1622 (2021). https://doi.org/10.1007/s12298-021-01029-8
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DOI: https://doi.org/10.1007/s12298-021-01029-8