Abstract
As a prelude to exploit DNA methylation-induced variation, we hypothesized the existence of substantial natural DNA methylation variation and its association with economically important traits in dolichos bean, and tested it using amplified methylation polymorphism-polymerase chain reaction (AMP-PCR) assay. DNA methylation patterns such as internal, external, full and non-methylation were amplified in a set of 64 genotypes using 26 customized randomly amplified polymorphic DNA (RAPD) primers containing 5′CCGG3′ sequence. The 64 genotypes included 60 germplasm accessions (GA), two advanced breeding lines (ABLs) and two released varieties. The ABLs and released varieties are referred to as improved germplasm accessions (IGA) in this study. The association of DNA methylation patterns with economically important traits such as days to 50% flowering, raceme length, fresh pods plant−1, fresh pod yield plant−1 and 100-fresh seed weight was explored. At least 50 genotypes were polymorphic for DNA methylation patterns at 10 loci generated by seven of the 26 RAPD primers. The GA and IGA differed significantly for total, full and external methylation and the frequency of methylation was higher in GA compared to that in IGA. The genotypes with external methylation produced longer racemes than those with full, internal and non-methylation in that order at polymorphic RAPD-11–242 locus. High pod yielding genotypes had significantly lower frequency of full methylation than low yielding ones. On the contrary, the genotypes that produced heavier fresh seeds harboured higher frequencies of total and externally methylated loci than those that produced lighter fresh seeds.
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References
Bender J (2004) DNA methylation and epigenetics. Annu Rev Plant Biol 55:41–68. https://doi.org/10.1146/annurev.arplant.55.031903.141641
Bulut B, Aydinl Z, Turktas M (2020) MSAP analysis reveals diverse epigenetic statuses in opium poppy varieties with different benzy isoquinoline alkaloid content. Turkish J Biol 44(2):103–109. https://doi.org/10.3906/biy-1911-69
Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Mol Genet Genomics 268:543–552. https://doi.org/10.1007/s00438-002-0772-4
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Eichten SR, Ellis NA, Makarevitch I, Yeh CT, Gent JI, Guo L, Mcginnis KM, Zhanh X, Schnable PS, Vaughn MW, Dawe RK (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8(12):e1003127. https://doi.org/10.1371/journal.pgen.1003127
Federer WT (1956) Augmented (or hoonuiaku) designs. Biometrics Unit. Cornell Univ. Mimeo. BU-74-M, February.
Fuller DQ (2003) African crops in prehistoric South Asia: a critical review. Food, fuel and fields: Progress African Arch Bot 239–271.
Fulnecek J, Kovarik A (2014) How to interpret methylation sensitive amplified polymorphism (MSAP) profiles. BMC Genet 15(1):2. https://doi.org/10.1186/1471-2156-15-2
Gallusci P, Dai Z, Genard M, Gauffretau A, Leblanc-Fournier N, Richard-Molard C, Vile D, Brunel-MuUGUET S (2017) Epigenetics for plant improvement: current knowledge and modelling avenues. Trends Plant Sci 22(7):610–623. https://doi.org/10.1016/j.tplants.2017.04.009
Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B, Laga B (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc Natl Acad Sci 106(47):20109–20114. https://doi.org/10.1073/pnas.0908755106
Hofmeister BT, Lee K, Rohr NA, Hall DW, Schmitz RJ (2017) Stable inheritance of DNA methylation allows creation of epigenotype maps and the study of epiallele inheritance patterns in the absence of genetic variation. Genome Biol 18(1):1–16. https://doi.org/10.1186/s13059-017-1288-x
Hu Y, Morota G, Rosa GJ, Gianola D (2015) Prediction of plant height in Arabidopsis thaliana using DNA methylation data. Genetics 201(2):779–793. https://doi.org/10.1534/genetics.115.177204
Iwasaki M, Paszkowski J (2014) Epigenetic memory in plants. The EMBO J 33(18):1987–1998. https://doi.org/10.15252/embj.201488883
Karaca M, Aydin A, Ince AG (2019) Cytosine methylation polymorphisms in cotton using TD-MS-RAPD-PCR. Mod Phytomorphol 13:14–18
Kay DE. (1975) Food legumes, TPI crop and product digest No. 3. Lablab purpureus. Hyacinth bean: 184–196
Kellenberger RT, Schluter PM, Schiestl FP (2016) Herbivore-induced DNA demethylation changes floral signalling and attractiveness to pollinators in Brassica rapa. PLoS ONE 11(11):e0166646. https://doi.org/10.1371/journal.pone.0166646
Keyte AL, Percifield R, Liu B, Wendel JF (2006) Infraspecific DNA methylation polymorphism in cotton (Gossypium hirsutum L.). J Hered 975(444):450. https://doi.org/10.1093/jhered/esl023
Kumar S (2019) Epigenomics for crop improvement: current status and future perspectives. J Genet Cell Biol 3:128–134
Kumar SA, Singh A (2016) Epigenetic regulation of abiotic stress tolerance in plants. Adv Plants Agric Res 5:00179. https://doi.org/10.15406/apar.2016.05.00179
Kumar S, Singh AK, Mohapatra T (2017) Epigenetics: history, present status, and future perspective. Indian J Genet 77:445–463. https://doi.org/10.5958/0975-6906.2017.00061.X
Liu R, How-Kit A, Stammitti L, Teyssier E, Rolin D, Mortain-Bertrand A, Halle S, Liu M, Kong J, Wu C, Degraeve-Guibault C (2015) A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc Nat Acad Sci 112(34):10804–10809. https://doi.org/10.1073/pnas.1503362112
Magoon ML, Singh A, Mehra KL (1974) Improved field bean for dryland forage. Indian Farming 24(2):5–7
Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nat 461(7267):1135–1138. https://doi.org/10.1038/nature08498
Melquist S, Luff B, Bender J (1999) Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genet 153(1):401–413
Miura K, Agetsuma M, Kitano H, Yoshimura A, Matsuoka M, Jacobsen SE, Ashikari M (2009) A meta stable DWARF1 epigenetic mutant affecting plant stature in rice. Proc Natl Acad Sci 106(27):11218–11223. https://doi.org/10.1073/pnas.0901942106
Nene YL (2006) Indian pulses through the millennia. Asian Agri-History 10(3):179–202
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel Population genetic software for teaching and research–an update. Bioinformatics 28(19):2537. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Phutikanit N, Suwimonteerabutr J, Harrison D, D’occhio M, Carroll B, Techakumphu M (2010) Different DNA methylation patterns detected by the Amplified Methylation Polymorphism Polymerase Chain Reaction (AMP PCR) technique among various cell types of bulls. Acta Vet Scand 52(1):1–9. https://doi.org/10.1186/1751-0147-52-18
Quadrana L, Almeida J, Asis R, DUFFY T, DOMINGUEZ PG, BERMUDEZ L, CONTI G, DA SILVA JVC, PERALTA IE, COLOT V, ASURMENDI S (2014) Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat Communication 5(1):1–11. https://doi.org/10.1038/ncomms5027
Raju SKK, Shao MR, Sanchez R, Xu YZ, Sandhu A, Gtaef G, Mackenzie S (2018) An epigenetic breeding system in soybean for increased yield and stability. Plant Biotechnol J 16(11):1836–1847. https://doi.org/10.1111/pbi.12919
Ramesh S, Byregowda M (2016) Dolichos bean (Lablab purpureus L Sweet var Lignosus) genetics and breeding-present status and prospects. Mysore J Agric Sci 503(481):500
Richards CL, Schrey AW, Pigliucci M (2012) Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with high epigenetic differentiation. Ecol Letters 15:1016–1025. https://doi.org/10.1111/j.1461-0248.2012.01824.x
Riddle NC, Richards EJ (2002) The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162(1):355–363
Salmon A, Clotault JA, Jenczewski EB, Chable VA, Maria J, Manzanares-Dauleux A (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci 174:61–70. https://doi.org/10.1016/j.plantsci.2007.09.012
Schmitz RJ, Schultz MD, Lewsey MG, O’malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR, (2011) Trans-generational epigenetic instability is a source of novel methylation variants. Sci 334(6054):369–373. https://doi.org/10.1126/science.1212959
Schultz R, Eckstein L, Durka W (2013) Scoring and analysis of methylation-sensitive amplification polymorphisms for epigenetic population studies. Mol Ecol Resour 13:642–650. https://doi.org/10.1111/1755-0998.12100
Sha AH, Lin XH, Huang JB, Zhang DP (2005) Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation sensitive AFLP (MSAP) analysis. Mol Genet Genomics 273(6):484–490. https://doi.org/10.1007/s00438-005-1148-3
Singh KP (2014) Screening of DNA methylation changes by methylation-sensitive random amplified polymorphic DNA-polymerase chain reaction (MS-RAPD-PCR). In Mol Technology Protocols 71-81. https://doi.org/10.1007/978-1-62703-739-6_6
Springer NM, Schmitz RJ (2017) Exploiting induced and natural epigenetic variation for crop improvement. Nat Rev Genet 18(9):563. https://doi.org/10.1038/nrg.2017.45
Seymour DK, Becker C (2017) The causes and consequences of DNA methylome variation in plants. Curr Opin Plant Biol 36:56–63. https://doi.org/10.1016/j.pbi.2017.01.005
Shen Y, Zhang J, Liu Y, Liu S, Liu Z, Duan Z, Wang Z, Zhu B, Guo YL, Tian Z (2018) DNA methylation footprints during soybean domestication and improvement. Genome Biol 19(1):1–14. https://doi.org/10.1186/s13059-018-1516-z
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21(1):64
Tirnaz S, Batley J (2019) Epigenetics: potentials and challenges in crop breeding. Mol Lant 12(10):1309–1311. https://doi.org/10.1016/j.molp.2019.09.006
Wei X, Song X, Wei L, Tang S, Sun J, Hu P, Cao X (2017) An epiallele of rice AK1 affects photosynthetic capacity. J Integrative Plant Biol 59(3):158–163. https://doi.org/10.1111/jipb.12518
Weigel D, Colot V (2012) Epialleles in plant evolution. Genome Biol 13(10):1–6. https://doi.org/10.1186/gb-2012-13-10-249
Yan W (1999) Methodology of cultivar evaluation based on yield trial data-with special reference to winter wheat in Ontario. Doctor Philosophy Thesis submitted to University of Guelph, Ontario, Canada.
Yang BZ, Zhang H, Ge W, Wender N, Douglas-Palumberi H, Perepletchikova F, Gelernter J, Kaufman J (2013) Child abuse and epigenetic mechanisms of disease risk. American J Prev Med 44(2):101–107. https://doi.org/10.1016/j.amepre.2012.10.012
Yi C, Zhang S, Liu X, Bui HT, Hong Y (2010) Does epigenetic polymorphism contribute to phenotypic variances in Jatropha curcas L. BMC Plant Biol 10(1):259. https://doi.org/10.1186/1471-2229-10-259
Zhang X, Sun J, Cao X, Song X (2015) Epigenetic mutation of RAV6 affects leaf angle and seed size in rice. Plant Physiol 169(3):2118–2128. https://doi.org/10.1104/pp.15.00836
Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, Yu Y, Shu L, Zhao Y, Ma Y, Fang C (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33(4):408–414. https://doi.org/10.1038/nbt.3096
Zhang L, Cheng Z, Qin R, Qiu Y, Wang JL, Cui X, Gu L, Zhang X, Guo X, Wang D, Jiang L (2012) Identification and characterization of an epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell 24(11):4407–4421. https://doi.org/10.1105/tpc.112.102269
Zhang Y, Wendte JM, Ji L, Schmitz RJ (2020) Natural variation in DNA methylation homeostasis and the emergence of epialleles. Proc National Acad Sci 117(9):4874–4884. https://doi.org/10.1073/pnas.1918172117
Zhao Y, Yu S, Xing C, Fan S, Song M (2008) Analysis of DNA methylation in cotton hybrids and their parents. Mol Biol 42(2):169. https://doi.org/10.1134/S0026893308020015
Zheng X, Hou H, Zhang H, Yue M, Hu Y, Li L (2017) Histone acetylation is involved in GA-mediated 45S rDNA de-condensation in maize aleurone layers. Plant Cell Rep 37(1):115–123. https://doi.org/10.1007/s00299-017-2207-z
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We gratefully acknowledge financial support from Indian Council of Agricultural Research (ICAR)—World Bank funded project to carry-out part of the research (ICAR_NAHEP; F. No./NAHEP/CAAST/2018–19/08).
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SR and CA conceptualized the research. HA executed the complete investigation and prepared draft manuscript. NCS curated and analysed the data, and prepared tables and graphs. SR reviewed, edited and finalized the manuscript.
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Ajaykumar, H., Ramesh, S., Sunitha, N.C. et al. Assessment of natural DNA methylation variation and its association with economically important traits in dolichos bean (Lablab purpureus L. Var. Lignosus) using AMP-PCR assay. J Appl Genetics 62, 571–583 (2021). https://doi.org/10.1007/s13353-021-00648-x
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DOI: https://doi.org/10.1007/s13353-021-00648-x