Key words: cultivated inBrazil. genetic diversityandtheoriginoflimabeanlandraces programs, since currently thereis little information on the resultswillbeusefultobreedingtwo genepools.Our another groupwithintermediatecharacteristicsofthese typical oftheMesoamericanand Andean genepools,and showed thepresenceofaccessionswithcharacteristics to genetic divergence among the accessions. Results length andwidthcharacteristicswerethemaincontributors germplasm. High genetic variability was detected and seed organization ofthegeneticdiversityandoriginthis MLM (ModifiedLocationModel)inordertoanalizethe qualitative and quantitative descriptors through the Ward- 166 accessionsofcultivatedlimabeanfromBrazilusing diversity andoriginofthiscrop. We aimedtocharacterize traits, whichareimportantforunderstandingthegenetic It hasahighdegreeofphenotypicvariationforseed it isanalternativeincomeinadditiontoafoodsource. has agreatrelevance,mainlyintheNortheast,where amino acidsnecessaryforhumans.InBrazil,limabean of protein for people as it contributes all of the essential Lima bean( ABSTRACT analysis, morphologicalmarkers, doi:10.4067/S0718-58392017000100004 Accepted: 31December2016. Received: 28 August 2016. 97200, ColoniaChuburnádeHidalgo, Mérida, Yucatán, México. 4 Petrônio Portela,Ininga,64049-550, Teresina, Piauí,Brasil. 3 Norte (final),70770-900,Brasilia,DF, Brasil. Genéticos eBiotecnologia, Parque Estação Biológica - PqEB Av. W5 2 Brasil. Ferreira Sobral,BR343,km3,5.Meladão 64800000, Floriano,Piauí, 1 Raimundo Nonato Oliveira Silva strategy cultivated inBrazil, usingtheWard-MLM Phenotypic diversity inlimabeanlandraces Ângela Celis deAlmeidaLopes and JaimeMartínez-Castillo Centro de Investigación Científica de Yucatán, Calle 43 No. 130, C.P. Universidade FederaldoPiauí,CampusUniversitário Ministro Empresa Brasileira de Pesquisa Agropecuária, Embrapa Recursos Universidade FederaldoPiauí,CampusUniversitário Amílcar CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY * Correponding author([email protected]). Phaseolus lunatus Breeding, germplasm characterization, CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY L.)isanimportantsource Phaseolus lunatus 4 3 , Regina Lucia Ferreira Gomes 1* , MaríliaLobo Burle .
joint - MARCH 2017 2 Lima bean( INTRODUCTION varieties: var. origin ofthisgermplasm. the explore to and characters phenological and morphological accessions from Brazil through the Ward-MLM procedure using the organization ofthegeneticdiversitypresentin limabean Castillo etal.,2008;2012; 2014). Ourobjectivesweretotest a centerofdiversityfortheMesoamericangenepool(Martínez- as considered region a Yucatanthe Peninsula, in reported that as landraces and morphological variation ofseed,could be ashigh of number the in reflected diversity, genetic the that show have et al.,2008;Silva2015).Collections obtained fromBrazil and analternative income source forthe local population (Santos importance in theNortheastofBrazil,whereitisusedasafood as fava, favabelém orfeijão-de-lima, and it has considerable known is bean lima Brazil, In 1998). al., et (Lioi Africa and important sourceofproteinforruralpopulationsinSouth America the genus (Santos etal.,2010). pools and later to characterize the genetic diversity of this species gene main the recognize to used firstly was aspect This 1994). high levelofpolymorphism,mainlyrelatedtoseedtraits(Lioi, Potato represent the MIand MIIgene pools. Lima bean has a and Sieva while pool, gene the A represents Lima Big seeds. flat 2) Potato, with small globular seeds; and3)Biglima, with large seeds; flat and medium-sized with Sieva, 1) cultigroups: three of Within thevar. hipotesis. this explore limits America South from collections Castillo, personal communication), but lack of wild lima bean possible domestication event in South America (Jaime Martínez- evidence frommicrosatellite markers havesuggested another (Andueza-Noh etal.,2013;2015).Recent and CostaRicaforMII etal.,2013);and3)theregionlocatedbetweenGuatemala Noh Andueza- 2012; al., et (Serrano-Serrano MI for Mexico from region eastern central the 2) 1997); al., et (Maquet America altitude western valleys between Ecuador and Peru in South one domestication event in each of them: 1) for A, the mid- (A) and two Mesoamerican gene pools (MIand MII); with pool gene Andean One pools: gene major three of existence the indicated have Studies 1977). (Baudet, one domesticated the , JulianoGomesPádua As acrop,limabeanisthesecondmostimportantlegumeof 3 , Phaseolus Phaseolus lunatus - silvester MARCH 2017 lunatus on the world (Maquet et al., 1999). It is an is It 1999). al., et (Maquet world the on forthewildmaterialandvar. , Baudet (1977) indicated the existence the indicated (1977) Baudet , 2 , L.)iscomposedoftwobotanical lunatus for
35 RESEARCHRESEARCH CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY CV % Mean Error beans from EmbrapaGeneticResources andBiotechnology, Brasilia-DF, 2010. Table 1.Estimatesofmeansquares obtained intheanalysisofvariance of thecharacteristics evaluated for 166accessionsoflima of genotypesconservedingenebanks,especiallywith classification the for important is approach of type This interpreted abignumberofcharacterssimultaneously. variables wasanalyzedbyFtestat5%probability. quantitative the of significance The caliper. digital a using determined were (mm) measures The (GH). habit growth and (CP), curvature pod (PST), tegument seed the of pattern pattern seedcolor(PSC),second(SSC), (SC), color seed (SP), profile seed (SS), shape seed were: used variables qualitative eight The g). (W100S, seeds 100 the meanthicknessof10randomseeds;and8)weight - mm) (TS, seed the of thickness 7) seeds; random 10 of selected seeds;6)seedwidth(SW, mm)-themeanwidth 5) seed length (SL, mm) -mean length of10randomly of seeds perpod, measured randomly in 10mature pods; pods; 4)numberofseedsperpod(NSP)-average number per pod (NLP)-number of locules in 10 randomly sampled width of10maturepodsatrandom;4)numberlocules (PW,maximum width the pod including 3) measured - mm) measured the longest straight line to the base of the tip pod); random were measured (in the case ofcurvedpods,we at pods mature 10 - mm) (PL, length pod 2) flowering; in first emergence to the stage where 50% of the plot was emergence to flowering (Flo, d) - number of days from quantitative variables used were:1) number ofdaysfrom eight The 1982). IBPGR, Italy; Rome, Resources, International (InternationalBoardforPlantGenetic traits were evaluated as recommended by Biodiversity disease controlwasperformedwhennecessary. and abamboostake.Insect thinning andhelduprightwith were sownper pot, which were reduced to one plant after in pots in a completely randomized design. Four seeds sown accessions the of replicates two Brasilia-DF,with in located greenhouse a in conducted was experiment The(CIAT, Colombia). TropicalAgriculture Cali, for and nineaccessions obtained from theInternational Center in different localitiesfromfivemainregionsBrazil, Embrapa Genetic Resources and Biotechnology, collected of Bank Germplasm by provided accessions 157 The A total of 166lima bean accessionswereusedinthisstudy. MATERIALS ANDMETHODS Accessions Source ** of seedsperpod;SL:seedlength;SW: seedwidth; TS: thickness oftheseed;CV: coefficientofvariation. number NSP: pod; per locules of number NLP: PW: width; length; pod pod PL: flowering; emergenceto from days of number Flo: freedom; of Degrees DF: Significant atthe 0.01 probabilitylevelintheFtest. At present,multivariateanalysispermittohandleand Eight quantitativedescriptorsandeightqualitative 166 165 DF 1474.07 95.87 63.19 Flo 8.29 d ** 435.32 64.30 12.49 PL 5.49
** 14.00 mm - MARCH 2017 14.46 7.10 1.05 PW Mean squares
** 0.25 SAS program(version9.0). Institute). Statisticalanalyzeswereperformedusingthe (SAS procedure CANDISC the by verified were that correlation ofcharacteristicswithcanonicalvariables criteria that show the differences between groups and performed accordingtothepseudoFand pseudot Gower’s algorithm(Gower, 1971). by provided was matrix distance the method, clustering (SAS Institute,Cary, NorthCarolina,USA).Forthe Ward 9.0 version program IMLSAS and the cluster of procedures MLM procedurefortheformationofgroupsthrough variables wereanalyzedsimultaneously, using the Ward- in limabean.Inthisstudy, thequantitative andqualitative used previously been not has that approach an is and 1971), defines groupsby the Gower dissimilarity algorithm (Gower, It 1963). Junior,(Ward method Ward’sclustering using (1998), al. et Franco by proposed procedure Ward-MLM the is analysis data for strategy joint This jointly. them in statistical techniques and freesoftwareneeded to analyze and qualitative variables stemsfromthelackofknowledge showed that limited use ofmethods usingbothquantitative of variabilityingermplasmbanks.Gonçalvesetal.(2008) qualitative variables is a potentially more complete indicator separately, although the joint analysis of quantitative and usually considerqualitativeorquantitativecharacteristics analyses Multivariate 2009). al., et Gonçalves 2008; al., et (Ortiz the recentadvancesincomputertechnology semi-climbing and6.02%showeddeterminategrowth indeterminate climbing growth habit, 12.05% indeterminate results. by environmental, thus conferringreliability to theobtained indicated thatcharacteristicsevaluatedwerelittleaffected all thevariables,indicatinggoodexperimentalprecisionand (number ofseeds per pod),which was considered low for 9.29 to length) (pod 5.49 from ranged obtained (CVs) variation of coefficients The accessions. studied the among variability genetic of existence the implies which (Table1), lima beanaccessions(P <0.01)forthemeansofalltraits different the among observed were differences Significant RESULTS ANDDISCUSSION The definition of the ideal number of groups was groups of number ideal the of definition The Of all accessiones analyzed, 81.93% of them had an had them of 81.93% analyzed, accessiones all Of 8.41 2.79 0.05 NLP **
0.26 9.29 2.76 0.07 NSP **
12.38 15.72 8.17 1.02 SL
** 5.04 mm 6.79 9.15 0.39 SW
** 0.83 7.86 5.55 0.19 TS ** 2
36 of pseudoFandt group. Nevertheless, focusshouldbegiventolarger values mean vectors ofthe two clusters jointed to form a new in which each clustering step is related to a test to compare groups inacluster analysis, are similar to ahypothesistest that the numberofgroupscanvaryaccording to thespecies, indicated (2009) al. et Gonçalves group. different another vectors arerejected, twogroupswillnotbeunitedagain in of means with major significance. Iftheequality of mean andrejectingtheequality significance probability oftest CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY to thepseudoFandt according groups three of existence the indicated procedure Ward-MLMThe 3). (Table rose 0.60% and yellow and black, 4.82%lightbrown,4.22%red-purple,1.20%gray 7.23% red, 10.84% cream, 18.07% white, 22.29% brown, 29.52% verified: was variability wide a (SC), color seed (Tablefor respectively 2). As seeds, of width and length for mm 14.17 to 6.54 from and mm 22.53 to 8.28 from values traits, thisstudyshowedwidemorphological variation, with seed For 2). (Table width and length seed were variability the characteristics that contributed most to the genetic genetic diversity(Vargas etal.,2003).Inthisstudy, and origin their explain to used criteria main the of one study ofthe morphological variation ofseeds has been among the lima bean consumers. Inlima beans,the that larger podscontain large seeds, which ispreferred BF113. Inlima bean it is animportant feature, considering average valueofpodlengthwasobservedingenotype highest The mm. 64.33 of average an with mm, 129.17 and 42.50 between ranged characteristic, that for exists and 26d,respectively. 31 30, 30, 30, 30, 31, 41, 34, 41, 40, 39, 37, 49, 40, 48, 35, 40, with G27059 and G26222 G26200, G25633, G25165, G25143, G25142, G25140, G25137, BF206, BF205, BF202, BF201, BF199, BF133, BF132, BF87, BF7, were: accessions Brazil. These in studies on literature the in found accessions showed shorter cycles in comparison with the among the evaluated accessions. Concerning to this trait, 18 ranged between26 and 153 d, showing a wide variability flowering to emergence from days of number The habit. t from theEmbrapaGeneticResources beans andBiotechnology, lima Brasilia-DF, of 2010. accessions 166 from determined (CAN1), variable canonical first the and Ward-MLMstrategy the by formed GIII) Table 2. Values ofmaximum,minimum, andaveragefor thequantitativecharacteristics for eachofthethree groups(GI andGII, Flo: Numberofdays fromemergence toflowering;PL:podlength;PW: podwidth;SL: seed length;SW: seedwidth; W100S:weight of 100seeds. W100S, g SW, mm SL, mm PW, mm PL, mm Flo, d Characters 2 tests,whichdeterminetheidealnumberofaccessions Regarding thepodlengthtraittherewidevariability According toMingoti(2005),thepseudoFand Maximum 147.03 129.17 153.00 13.56 21.35 9.76 Minimum 2 17.52 42.50 78.00 , sincetheyarerelated to theleast GI 6.54 8.28 8.40 2 criteria. 108.01 Medium 34.25 10.89 13.50 58.33 8.23 Maximum 112.00 72.00 17.95 20.36 93.05 11.70 - MARCH 2017 Minimum 17.89 45.67 26.00 GII Group 7.16 8.58 9.58 Growth habit(GH) Seed size(SZ) Seed profile(SP) Seed shape(SS) Pattern seedcolor(PSC) Seed color(SC) showed bycultivatedaccessionsfromtheMesoamerican characteristics foundinthisgrouparesimilartothose The seeds. of width and length for values mean lowest trait, withsmall,semi-flattenedandsphericalseeds, higher meanvaluesforthenumberofdaystoflowering had that accessions the comprised group This accessions). for groupformationresultsinlesssubjectivegroups. However, thesameauthorsnotedthatmore precisecriteria number of accessions and number and type of descriptors. and Biotechnology, Brasilia-DF, 2010. accessions oflima beans from theEmbrapaGenetic Resources 166 the from WARDstrategy the ‑MLM by formed GIII) and qualitative characteristics,ineachofthethree groups(GI, GII, Table 3. Variables and number of accessions by group of Variables Indeterminate climbing Indeterminate semi-climbing Determinate shrubby Large Medium Small Full Semi-flat Flat Oblong Elliptical Spherical Black Red Dark Brown Light brownororange Absent Another Black Red-Purple Red Rose Brown Light Brown Yellow Gray White Group I contained the highest number of accessions (74 accessions of number highest the contained I Group Medium 32.83 13.73 59.62 72.02 11.47 8.73 Maximum 122.50 151.00 92.45 14.17 22.53 27.32 Minimum 35.79 12.98 10.12 57.44 37.00 GIII GI (74) 9.29 60 13 46 27 26 42 10 63 13 10 45 15 123 12 25 11 1 1 6 1 1 5 1 4 1 5 - -
Medium 60.68 16.94 16.94 80.49 99.90 11.17 GII (51) Group 40 20 13 31 22 23 41 46 20 12 20 22 14 10 11 15 2 9 6 - 1 4 20 4 3 9 6 1 10 2 1 4 2 3 2 2 - - 28 -
-0.130 CAN1 GIII (41) 0.431 0.899 0.912 0.637 0.624 36 13 5 3 ------
37 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY 87.86% of the total variation and report that high values high that report and variation total the of 87.86% procedure on common bean ( procedure oncommon dispersion analysis.Cabralelal.(2010),usingthesame genetic variabilityamongaccessionsevaluatedbygraphic methodology (Figure1),andenabledtovisualizethe variation amonggroups,obtainedbythe Ward-MLM total the of 99.0% explained variables canonical two first The 2). (Table characters the of variation of range the by showed bycultivatedaccessionsfromthe Andean genepool. those to similar are group this in found characteristics The obtained fromtheGermplasmBankofEmbrapalimabean. to groupIIIweresignificantlydifferent fromtheothers belonging accessions that observed was it Thus, (1991). al. et Castiñeiras and (1977) Baudet to according large, as classified mostly are seeds whose accessions has group This 2). (Table flat all are which seeds, the of width and length formed by accessions with the highest mean values for the the Mesoamericanand Andean genepools.GroupIIIwas seed characteristicsfoundinthisgroup,itisintermediateto CIAT.the from coming accessions all including Considering BF206, and BF205 BF203, BF179, BF133, BF87, BF7, lessthan60d,suchas studyhavevalues evaluated inthis accessions than60d.Many ofless values with lima beans were notreportsintheBraziliangermplasmaccessionsof and they perform well in crop rotation. Until now, there susceptible totheactionofpestsanddiseases,theycostless, from emergence toflowering.Earlygenotypesareless with short cycles, as indicated in the early number of days mechanized harvesting. Also, groupIIcomprisedaccessions for allows which work, hand excessive or staking require indeterminate growthhabit,theyrequirelesscareanddonot although they reach lower production compared with the number of days toflowering and maturity. Furthermore, type of growth habit in lima bean are more uniform in the this to Accessions habit. growth determinate of (90%) gene pool.GroupIIbroughttogethernearlyallaccessions the study. MLM strategy, considering166limabean accessionsusedin Ward- the with formed (G1-G3) groups three the of CAN2) and (CAN1 variables canonical two first the of Plot 1. Figure High variability was observed within groups as seen groupsas within observed variabilitywas High
P.vulgaris L.),obtained - MARCH 2017 chinense of thespecies morpho-agronomic descriptors,andobservedtheseparation of56 genetic diversity origin as a different cluster. Sudré et al. (2010) studied genetic variability, from theaccessions separating Andean Brazil using10morpho-agronomictraits,theydetectedhigh ( bean common of accessions 57 studied (2009) al. et Gonçalves evaluation. visual the on based refinement andacomplementfortheracialclassification additional an be may and accessions the classifies soundly descriptors, and concluded that the Ward-MLM procedure agronomic six using ofPeru fromhighaltituderegions races worked with50accessionsofeightmaize( using morphological and agronomic data. Ortiz et al. (2008) divergence andtoclustergenotypesbysimultaneously statistical procedureisausefultechniquetodetectgenetic among groupsandaccessionsinsidethesamegroup. canonical variables is adequate to verify the relationship ofthefirsttwoindicates thatthegraphicrepresentation be adomesticationcenter forthelimabean.Since could Brazil that is II group the of existence the about pools thanbetweenwildforms. differentiation gene observed betweenlandracesofthetwo authors, thishypothesisispartly supportedbythelower diversity ascomparedtowildforms. According tothese ingenetic causeanincrease would which of outcrossing), species is predominantly autogamous with variable levels the two gene pools through cross-hybridizations (the between genetic exchange to prone more be may landraces genetically differentiated. However, theysuggestedthat wild formsandlandraces, within each gene pool, are that showed markers, RAPD using (1997), al. et Fofana and Mesoamericangenepoolsare growing sympatrically. be actingasahybridzonewherelandracesfromthe Andean can Brazil that is II group the of existence the to explanation between both gene pools before mentioned. One possible characteristics intermediate with II group a of existence the and Andean domesticationcenters.Ourresultsalsoindicated Mesoamerican the from accessions of Brazil in existence the infer to us allowed result This pool. gene Andean the in group IIIshowedmorphologicalcharacteristicsobserved characteristics typicaloftheMesoamericangenepooland In the present study, group Ishowed morphological simultaneously fromquantitativeandqualitativevariables. detect genetic divergence and to cluster genotypes using data MLM statistical procedure proved to be a useful technique to Ward-The Brazil. in crop this for incipient still are studies breeding programs, considering that genetic and breeding landraces foundinthepresentstudyisgreatlyimportantfor bean lima of group each within present diversity genetic The germplasm Implications for theoriginof Several studies have shownthat the Ward-MLM Another, and perhaps more interesting explanation interesting more perhaps and Another, indifferent groups. C. annuum Capsicum , C. frutescens spp. accessionsusing26 spp. , C. baccatum P. vulgaris Zea mays and ) from L.) C. C.
38 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY evaluated. the most to genetic divergence between the accessions and widthwerethecharacteristics thathavecontributed domestication: Mesoamerican and Andean. Seedlength BF113 andG25633A. and thelongestdistance foundwasbetween accessions Genetic divergence wasfoundinthelima bean accessions, CONCLUSIONS (2015) analyzing10microsatellite Andean gene pools. More recently, Andueza-Noh etal. group present in the contact zone of the Mesoamerican and of intermediateformsrepresentingagenetically distinct occurrence the reported sequences, DNA repetitive simple to complementary oligonucleotides synthetic digoxigenated using (2002) Galasso and Lioi and rDNA, the of RFLP and diversity isozyme using (1998) al. et Lioi Also, (1986). Debouck by proposed diversity of center Andean northern and that thishypothesis could be consistent withthe domestication inthistransitionregioncanbesuggested distinct fromthosefarther north, indicatingthataformof landraces, the accessions from Costa Rica to Colombia are and forms wild mesoamerican among that observed (1997) of adomesticationeventenSud America. Fofana et al. existence the suggested authors ago, decades several beans throughplantbreeding. more productive, resistant and adapted varieties of lima the sourceofallelesinterest,whichallowsustoobtain consider we when essential becomes variability high This the Brazilian lima bean accessions maintained by Embrapa. Finally, ourresults showa wide range ofgenetic diversity in inter-microsatellites (ISSR) to confirm this hypothesis. orsecuences (SSR) microsatellites as molecular markers Castillo etal.,2008).Itisnecessarytomakestudiesusing (Martínez- Mexico in YucatanPeninsula the for indicated important centerofdiversityforthiscrop,as andBrazilcouldbean (asshowedinthisstudy), farmers in thelimabeanlandracescultivatedbyBrazilian be favoringthepresenceofhighlevelsgenetic diversity andthe from theMesoamerican could genepools Andean landraces of Brazil in presence the II, group of existence Andueza-Noh etal.,2013). 2012; al., et (Serrano-Serrano sequences DNA ribosomal and using moleculartechniques such as chloroplast and including more accessions (specially wild accessions) Sud America isnecessarytomakefurtherinvestigation to confirmthe hypothesis about a domesticationeventin American wildpopulationsstillnotcollected.However, American landraces may have been domesticated from Sud Sud the that suggesting it America, Central and Mexico related genetically with the wild populations collected in Mesoamerican landracescollectedinSud America arenot The accessions represent the two centers ofcenters two the represent accessions The Regardless ofthe hypothesis beforementioned about the loci observedthatthe - MARCH 2017 Lioi, L. 1994. Morphotype relationships in Lima bean ( bean Lima in relationships Morphotype 1994. L. Lioi, for Board International bean. Lima for Descriptors 1982. IBPGR. of some and similarity of coefficient general A1971. J.C. Gower, Júnior, R., A.T.,Amaral Karasawa, Rodrigues, L.S.A., Gonçalves, Junior, R., A.T.,Amaral Karasawa, Rodrigues, L.S.A., Gonçalves, Eberhart, and S., Taba,Villasenõr,J., J., Crossa, J., Franco, J.P.1997. Baudoin, P.,and Jardin, Vekemans,X., B., Fofana, of diversification Primary 1986. D.G. Debouck, 1991. A. Marino, and N., Rivero, M., Esquivel, L., Castiñeiras, Júnior, Amaral L.S.A., Gonçalves, T.C.B.,P.D.S.,Soares, Cabral, types cultivated the of status taxonomic The 1977. J.C. Baudet, M.L.,ChacónSánchez, Serrano-Serrano, R.H., Andueza-Noh, Andueza-Noh, R.H.,Martínez-Castillo, J.,and Chacón REFERENCES e Biotecnologiaforsupportthisresearch. supported by fellowships and Embrapa Recursos Genéticos Aperfeiçoamento dePessoalNívelSuperior(CAPES) for financialsupportofthisresearch.Coordenaçãode (CNPq-Brazil)Tecnológico e Cientíico Desenvolvimento deNacional Conselho to grateful are authors The ACKNOWLEDGEMENTS doi:10.1007/BF00053052. phaseolin. GeneticResources and CropEvolution41:81-85. lunatus Plant GeneticResources,Rome, Italy. its properties.Biometrics27:857-871.doi:10.2307/2528823. and MolecularResearch8:364-374.doi:10.4238/vol8-1gmr549. Genetics model. Ward-modifieda location using data molecular genetic divergence basedonmorphological,agronomic and M., and Sudré, C.P. 2009.Heirloom tomato gene bank: assessing Molecular Research7:1289-1297.doi:10.4238/vol7-4gmr526. algorithms toclustertomatoheirloom accessions.Geneticsand M., andSudré,C.P. 2008. Comparisonofmultivariate statistical doi:10.2135/cropsci1998.0011183X003800060045x. 38:1688-1696. Science Crop variables. continuous and categorical by resources genetic Classifying 1998. S.A. doi:10.1023/A:1002910114869. 95:157-165. Euphytica markers. RAPD by revealed as Genetic diversityinLimabean( 67:2-8. Newsletter Resources Genetic Plant centres? Three Americas: Jardín BotánicoNacional12:109-114. Variability of the seed of doi:10.1590/S0100-204X2010001000011. MLM strategy. Pesquisa Agropecuaria Brasileira 45:1124-1132. of thediversityamongcommonbeanaccessionsusing Ward- Quantification 2010. al. et R., A.B.P.,Lima, Rodrigues, A.T., Bulletin 7:29-30. of limabean( Evolution 60:1069-1086.doi:10.1007/s10722-012-9904-9. Crop and Resources Genetic sequences. DNA chloroplast gene pooloflimabean( J., etal.2013.MultipledomesticationsoftheMesoamerican M.I., Sánchez del Pino, I., Camacho-Pérez, L., Coello-Coello, 669. doi:10.1007/s10709-015-9863-0. 142:657- Genetica markers. microsatellite from evidence bean ( lima small-seeded of Domestication 2015. M.I. Sánchez, Phaseolus lunatus L.) deducedfromvariationofthe evolutionarymarker Phaseolus lunatus Phaseolus Phaseolus lunatus Phaseolus lunatus L.) landraces in Mesoamerica: L.) Tropical Grain Legume Grain Tropical L.) Phaseolus lunatus L. in Cuba. Revista L.):evidencefrom Phaseolus Phaseolus inthe L.)
39 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 77(1)JANUARY Mingoti, A.S. 2005. Análise dedadosatravésmétodos Martínez-Castillo, J., Colunga-GarcíaMarín, P., and Zizumbo- Martínez-Castillo, J.,Camacho-Pérez,L., Villanueva-Viramontes, Martínez-Castillo, J.,Camacho-Perez,L.,Coello-Coello,and Baudoin, and Wathelet,B., M., Delvaux, I., Bi, Zoro A., Maquet, Maquet, A., Vekemans, X.Z.,andBaudoin,J.P. 1999.Phylogenetic RFLPdiversity, Isozyme 1998. I. Galasso, and C., Lotti, L., Lioi, DNA Oligonucleotide 2002. I. Galasso, and L., Lioi, UFMG, BeloHorizonte,Brasil. estatística multivariada:umaabordagemaplicada.Editora 55:1065-1077. doi:10.1007/s10722-008-9314-1. diversity center. GeneticResourcesandCropEvolution Lima bean ( of conservation situ in and erosion Genetic 2008. D. Villarreal, ajb.1300412. doi:10.3732/ 101:851-864. Botany of Journal species. American markers: Implications for conservationanddomestication of the lunatus structure within the Mesoamerican gene pool of wild S., Andueza-Noh, R.H., and Chacón Sanchéz, I. 2014. Genetic Evolution 59:191-204.doi:10.1007/s10722-011-9675-8. Crop and Resources Genetic Mexico. Campeche, northeastern bean ( Andueza-Noh, R.H.2012. Wholesale replacement ofLima 991. doi:10.1007/s001220050651. 95:980- Genetics Applied and Theoretical markers. allozyme J.P. 1997. Genetic structure of a Lima bean base collection using Evolution 218:43-54.doi:10.1007/BF01087033. (Fabaceae), andimplicationsonitsorigin.PlantSystematics study onwild allies oflima bean, Evolution 213:153-164.doi:10.1007/BF00985196. beans, Lima cultivated among affinities phylogenetic and rDNA the of doi:10.1023/A:1013809915096. lunatus fingerprinting revealingpolymorphismin Phaseolus lunatus Phaseolus lunatus Phaseolus L. (Fabaceae) from Mexico as revealed bymicrosatellite L. Genetic Resources and Crop Evolution 49:53-58. Evolution Crop and Resources Genetic L. Phaseolus lunatus L.) landraces over the last 30 years in L. (Fabaceae). Plant Systematics and PlantSystematics L. (Fabaceae). L.) landraces inits Mesoamerican Phaseolus lunatus Phaseolus Phaseolus - MARCH 2017 L. L. Serrano-Serrano, M.L., R.H.,Martínez-Castillo,Andueza-Noh, Santos, J.O.,Gomes,R.L.F., Lopes, A.C.A., Silva,S.C.C.C., A.C.A.,R.L.F.,Lopes, A.S.F.,Gomes, Araújo, J.O., Santos, J. Burgueño, and R., Sevilla, J., Franco, J., Crossa, R., Ortiz, Ward Junior, J.H. 1963. Hierarchical grouping to optimize to grouping Hierarchical 1963. J.H. Junior,Ward Vargas, E.M., Castro, E., Macaya, G., and Rocha, O.J. 2003. C.P.,Sudré, R., L.S.A.,Rodrigues, Gonçalves, Júnior,Amaral A.T., Silva, V.B.,R.L.F.,Gomes, Lopes, C.T.S.,Dias, A.C.A., Silva, and domestication oflimabean( and Evolution 2012. M.I. Chacón, and D.G., Debouck, J., Cooperative 53:178-179. ( for physicalandchemicalcharactersofseedsinlimabean Bastos, E.M., Costa, E.M.R., et al. 2010. Genetic divergence Dynamic Soil,Plant2:56-60. Symbiosis: Importanceanddiversitytropicalsoils-areview. and Figueiredo,M.V.B. 2008.Rhizobia doi:10.1007/s10722-007-9224-7. plant traits.GeneticResourcesandCropEvolution55:151-162. 2008. Classification ofPeruvian highland maize races using Association 58:236-244.doi:10.1080/01621459.1963.10500845. an objective function. Journal of the American Statistical Rica. RevistadeBiología Tropical 51:707-724. of Variation inthesizeoffruits andseeds in38wildpopulations Molecular Research9:283-294.doi:10.4238/vol9-1gmr698. and Genetics analysis. statistical mixed in data agronomic and in domesticated Riva-Souza, E.M.,andBento,C.S.2010.Geneticvariability Agrárias 36:683-692.doi:10.5433/1679-0359.2015v36n2p683. in limabean( R.N.O. 2015. Genetic diversity and promising crosses indication doi:10.2135/cropsci2011.12.0642. 52:1698-1712. Science Crop DNA. ribosomal from Evidence Phaseolus lunatus Phaseolus lunatus Phaseolus lunatus Capsicum L.) Annual ReportoftheBeanImprovement (Fabaceae)fromCentral Valley ofCosta spp.asassessedbymorphological Phaseolus lunatus ) accessions.Semina.Ciências Phaseolus lunatus L.) in Mexico: in L.)
40