Confirmation of the relationship between

Confirmation of the relationship between plant height and Fusarium head blight resistance in wheat (Triticum aestivum L.)by QTL meta-analysisShuang-Lin Mao •Yu-Ming Wei •Wenguang Cao •Xiu-Jin Lan •Ma Yu •Zheng-Mao Chen •Guo-Yue Chen •You-Liang ZhengReceived:16July 2009/Accepted:7January 2010/Published online:16January 2010ÓSpringer Science+Business Media B.V.2010Abstract Fusarium head blight (FHB)is a serious wheat disease all over the world.In this study,the relationships between plant height (PH)and FHB were investigated across the whole wheat genome by QTL meta-analysis from fifty-six experiments.Coin-cident meta-QTL (MQTL)for PH and FHB were found on chromosomes 2D,3A,4B,4D and 7A.Rht-B1,Rht-D1,Rht8,MQTLs P7and P26were consis-tent with FHB MQTLs.The meta-analysis results confirmed the negative associations of Rht-B1,Rht-D1,and Rht8with FHB resistance.The associations of PH and FHB resistance on chromosomes 3A and 7A have not been reported and need further inves-tigation.These regions should be given attention in breeding programs.MQTLs derived from severalresistance sources were also observed.Some FHB MQTLs for different types of resistance overlapped.These findings could be useful for improving wheat varieties with resistance to FHB.Keywords Plant height (PH)ÁQTL ÁMeta-analysisIntroductionFusarium head blight (FHB)is a severe fungal disease of wheat (Triticum aestivum L.)in many areas of the world (Parry et al.1995).FHB not only causes significant yield losses,but also degrades grain quality.Mycotoxins deoxynivalenol (DON)and zearalenone,produced by the Fusarium spp.,that accumulate in FHB infected grains,are toxic to human and domestic animals when used as food and feed (Snijders 1990).FHB resistance is classified into five types (Mes-terha´zy 1995).More attention has been given to Types I,II and III.Type I is resistance to initial fungal pathogen infection;Type II resistance is resistance to fungal spread in the infected spike;and Type III is resistance to the accumulation of toxins in the grain.Heading date and morphological characters,including plant height (PH),presence of awns and spike compactness have been associatedwith FHB resistance in wheat (Mesterha´zy 1995;S.-L.Mao ÁY.-M.Wei Án ÁM.Yu ÁZ.-M.Chen ÁG.-Y.ChenTriticeae Research Institute,Sichuan Agricultural University,Ya’an,625014Sichuan,People’s Republic of ChinaS.-L.Mao ÁY.-M.Wei ÁM.Yu ÁZ.-M.Chen ÁG.-Y.Chen ÁY.-L.Zheng (&)Key Laboratory of Southwestern Crop Germplasm Utilization,Ministry of Agriculture,Ya’an,625014Sichuan,People’s Republic of China e-mail:ylzheng@W.CaoAgriculture and Agri-Food Canada,Eastern Cereals and Oilseeds Research Centre,960Carling Avenue,Ottawa,ON K1A 0C6,CanadaEuphytica (2010)174:343–356DOI 10.1007/s10681-010-0128-9Steiner et al.2004).It is generally accepted FHB resistance is positively related to PH,and the association has been observed for several chromo-somes(Gervais et al.2003;Steiner et al.2004; Somers et al.2003;Schmolke et al.2005;Draeger et al.2007;Srinivasachary et al.2008).Both PH and FHB resistance are complex traits controlled by polygenes,and QTLs have been located on nearly all 21chromosomes(Snape et al.1977;Buerstmayr et al. 2002).Meta-analysis is a method of combining data from different sources in a single study to reveal co-locations between genes and QTLs(Goffinet and Gerber2000;Arcade et al.2004).It has been successfully used in animal(Belknap and Atkins 2001)and plant QTL analysis(Chardon et al.2004; Hanocq et al.2007).After the consensus locations of traits are estimated,the association of each locus in the same linkage group are analyzed.The objective of this study was to investigate the relationships between PH and three types of FHB resistance across the whole wheat genome by meta-analysis. For this purpose,we collected numerous published QTL data on wheat PH and FHB reaction,and then used Meta-analysis to integrate all the data from independent experiments to conform‘real’QTL for both traits.Materials and methodsData collectionThirty studies published from1994to2009on wheat PH QTLs were collected;these had sufficient map-ping data to allow QTLs to be projected onto a consensus map.The genetic materials,numbers of QTL,population types and size of each population are listed in Table1.The population types included recombinant inbred lines(RIL),backcrossed lines (BC),doubled haploid lines(DH)and F2plant populations.The population sizes ranged from50 (Shah et al.1999)to460lines(Spielmeyer et al. 2007).Except for six studies(Korzun et al.1997, 1998;Shah et al.1999;Kato et al.1999;Araki et al. 1999;Spielmeyer et al.2007),the PH QTL analyses involved the entire genome.Data for35studies on FHB QTLs were collected and the QTLs are listed in Table2.Populations included BC,DH and RILs as test materials and the sizes of mapping populations ranged from51 (Cuthbert et al.2006)to318lines(Shen et al. 2003b).Each FHB QTL study scanned almost all21 chromosomes,except those of Shen et al.(2006), Handa et al.(2008)and Cuthbert et al.(2006,2007), who investigated FHB resistances on only one chromosome.In nine studies,both PH and FHB QTLs were analyzed(Bo¨rner et al.2002;Somers et al.2003;Gervais et al.2003;Paillard et al.2004; Steiner et al.2004;Schmolke et al.2005;Klahr et al.2007;Draeger et al.2007;Srinivasachary et al. 2008),but that of Klahr et al.could not be used for meta-analysis on PH due to insufficient common markers.QTL projectionsQTLs identified in one population evaluated in a given environment were defined as an experiment. The identified QTLs were projected onto a reference map for meta-analysis.The position,LOD score, confidence interval(C.I.)and proportion of pheno-typic variance(R2)of each QTL were used for projection.When the C.I.of a QTL was not documented,a95% C.I.was estimated using the approach of Darvasi and Soller(1997):C:I:¼530=NÃR2ÀÁwhere N is the population size and R2is the proportion of phenotypic variance explained by the QTL.A wheat composite map(Appels2004)was used as the reference map.The composite map,which integrated11mapping studies,contains3,741RFLP, AFLP and SSR markers covering a total length of 3,236cM with an average distance of0.76cM between markers.QTLs were projected to the reference map using BioMercator v2.1(Arcade et al.2005).First,the marker names of the initial maps were standardized according to the reference map.Then,the tools of map projection were used to project the QTLs onto the composite map.During the projection,reversed marker orders were found.If two inverted markers were closely linked(B1cM),one marker was removed manually.Otherwise,the inverted markers were discarded automatically by the software.However,some original maps or partial linkage groups(Cadalen et al.1998;Korzun et al.1998;Zhang and Mergoum2007;Wang et al.2009;Ahmed et al. 2000;Somers et al.2003;Zhang et al.2008;Yu et al. 2008b)with insufficient common markers could not be projected onto the reference map directly.In such cases,the wheat consensus map of Somers et al.(2004) was used as a transitional map.This map has large numbers of markers in common with the Appels(2004) reference map and enabled more precise projections.Table1Collated map and QTL information on plant heighta RIL recombinant inbred lines,BC backcrossed lines, DH doubled-haploid lines Number ofQTLCross PopulationsizePopulationtype aReferences23Opata9W7984114RIL Bo¨rner et al.2002 3Sicco9Highbury-HB114DH Hyne et al.1994 3CM189Vigour18460RIL Spielmeyer et al.20076RL44529AC Domain182DH McCartney et al.20052Grandin9BR34118RIL Liu et al.20055Prinze9W798472BC Huang et al.2003 9Arina9Forno240RIL Schnurbusch et al.200314Flair9Xx86111BC Huang et al.2004 4CA96139H1488113DH Hai et al.20081CS9Kanto1074A98BC Araki et al.1999 1Frontana9INIA66117RIL Ayala et al.2002 2Opata9W7984114RIL Ayala et al.2002 4Arina9Riband116DH Draeger et al.2007 4Savannah9Senat106DH Eriksen et al.2003 2Renan9Re´cital194RIL Gervais et al.2003 9Huapei39Yumai57168DH Zhang et al.2008 1CNN9CNN(WI3A)50RIL Shah et al.19997Courtot9CS275DH Cadalen et al.1998 2CS(Cappelle-Desprez5A)9CS(T.spelta5A)120F2Kato et al.19997CS9SP66RIL Ahmed et al.2000 5Kofa9Svevo249RIL Maccaferri et al.20084Wangshuiba9Alondra104RIL Zhou et al.2004a 5ND33389F390240RIL Liu et al.20021Bersee9W-800114F2Korzun et al.1997 1Cappelle9Cappelle(Mara2D)100F2Korzun et al.1998 4Spark9Rialto128RIL Srinivasacharyet al.20086Heshangmai9Yu8679142RIL Wang et al.2009 1Wuhan-19Maringa91DH Somers et al.2003 1Dream9Lynx145RIL Schmolke et al.200518Arina9Forno240RIL Paillard et al.2004 4Frontana9Remus210DH Steiner et al.2004QTL meta-analysisQTL meta-analysis was carried out for each chromo-some using sets of QTLs.It pools QTLs in independent experiments and provides a consensus position and C.I.for them.The consensus QTL positions are estimated as the mean QTL distribution maximum likelihood.The95%confidence interval ofTable2Collated map and QTL information on Fusarium head blightNumber of QTL Cross combination Population size Population type a Reference1Opata9W7984114RIL Bo¨rner et al.20021Wuhan-19Maringa91DH Somers et al.20037Annong84559Wangshuibai218RIL Ma et al.2006b2Ning8940379Alondra218RIL Shen et al.20063Ning8940379Alondra218RIL Shen et al.2003a10Alondra‘s’9Wangshuibai104RIL Zhou et al.2004b1Sumai39Stoa112RIL Anderson et al.20011ND26039Butte86139RIL Anderson et al.20012Sumai39Stoa112RIL Waldron et al.19992Ritmo9Cansas94RIL Klahr et al.20071Huapei57-29Patterson163RIL Bourdoncle and Ohm2003 1Ning78409Clark128RIL Yu et al.2008a11Arina9Riband116DH Draeger et al.20074Sumai39Gamenya118DH Handa et al.200815Renan9Re´cital194RIL Gervais et al.20031Sumai3*59Thatcher51BC Cuthbert et al.20061HC37493*98B69-L4766BC Cuthbert et al.200613DH1819AC174DH Yang et al.2005b13Spark9Rialto129DH Srinivasachary et al.2008 1CS-SM3-7ADS9Annong92RIL Ma et al.2006a1BW2789AC89RIL Cuthbert et al.20071Pelikan//Bussard9Ning8026122RIL Ha¨berle et al.200919Nanda24199Wangshuibai136RIL Lin et al.20065Alondra‘s’9Wangshuibai104RIL Zhang et al.200416Nanda24199Wangshuibai136RIL Lin et al.20044Dream9Lynx145RIL Schmolke et al.20054Sumai39Stoa239DH Zhang and Mergoum2007 2CM-820369Remus239DH Buerstmayr et al.20022Frontana9Remus210DH Steiner et al.20043Chokwang9Clark79RIL Yang et al.2005a18Arina9Forno240RIL Paillard et al.20044Veery9CJ9306152RIL Jiang et al.2007a4Veery9CJ9306152RIL Jiang et al.2007b6Alondra‘s’9Wangshuibai134DH Jia and Chen20054Patterson9F201R318RIL Shen.et al.2003b6Arina9NK9360493DH Semagn et al.200719Wheaton9Wangshuibai139RIL Yu et al.2008bResistant material derived from Sumai3shown in bold italica RIL recombinant inbred lines,BC backcrossed lines,DH doubled-haploid linesthe consensus QTL is deduced by the algorithm (Arcade et al.2004):C :I :¼3:92Ãffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi1.X1=r 2i ðÞr wherer i2is the variance of position of the ith QTL of the distribution.The BioMercator computes the consensus QTL by models 1,2,3,4and n.Model 1represents all the input QTLs in a single location on the linkage group.Model n means all the input QTLs in n different locations.The most likely model is the one minimizing the Akaike criterion (AIC value).However,the software defaults from model 4to a model with as many ‘real’QTLs as the input.Therefore,when there are over four consensus QTLs on the same linkage group,the method described by Chardon et al.(2004)was used to separate the QTLs in several groups before meta-analysis.ResultsMaps and QTL projectionA total 149PH QTLs and 221FHB QTLs wereobtained,whereas PH QTLs were distributed across the whole wheat genome,but with relatively fewer located on D genome chromosomes (5on 1D,7on 2D,3on 3D,9on 4D,2on 5D,5on 6D,3on 7D).FHB QTLs occurred on all chromosomes except 1D.Most chromosomes had both Type I and Type II FHB QTLs.A few chromosomes had Type III QTLs.One hundred and thirty-three PH QTLs were projected onto the reference map.Sixteen QTLs from 11experiments were projected onto chromosome 6A,11QTLs from 9experiments onto 5A,and 10QTLs from 9experiments onto 4B.The numbers of initial and projected QTLs concentrated on each chromo-some are listed in Table 3.Table 3Projected PH and FHB QTLs on the reference map Chromosome PH aQTLs-S Type II FHB resistance Type III FHB resistance 1A 5(5),5(5)1(1),1(1)3(3),3(3)2(2),2(2)1B 5(5),4(4)4(4),4(4)6(6),4(4)2(2),2(2)1D 4(5),3(4)–––2A 4(4),4(4)5(5),4(4)2(2),2(2)2(2),2(2)2B 7(11),7(10)4(4),3(3)6(6),2(2)–2D 5(7),5(6)8(8),5(5)6(8),4(6)2(2),2(2)3A 9(9),7(7)9(9),6(6)1(1),1(1)–3B 6(7),5(6)11(15),7(8)28(28),16(16)6(6),4(4)3D 3(3),3(3)3(3),2(2)2(2),2(2)–4A 9(9),4(4)4(4),3(3)1(1),1(1)–4B 10(12),9(11)6(7),3(4)1(1),1(1)–4D 5(9),5(8)5(5),3(3)2(2),2(2)1(1),1(1)5A 11(11),9(9)14(16),6(8)4(4),4(4)4(4),4(4)5B 4(4),4(4)10(10),4(4)––5D 2(2),1(1)2(2),2(2)3(3),2(2)1(1),1(1)6A 16(16),11(11)4(4),4(4)1(1),1(1)–6B 7(7),4(4)6(6),5(5)7(7),4(4)1(1),1(1)6D 4(5),4(5)4(4),2(2)––7A 6(6),5(5)7(7),6(6)2(2),1(1)1(1),1(1)7B 9(9),7(7)2(2),2(2)3(3),3(3)–7D2(3),2(3)1(1),1(1)1(1),1(1)1(1),1(1)anumber within parenthesis represents the number of initial QTL;number before parenthesis represents the number of projected QTL;‘‘–’’chromosome lacks a QTL;numbers within italic parenthesis represents the number of initial studies on the chromosome;italic number before italic parenthesis represents the number of projected studies on the chromosomeFHB QTLs for Type I,II and III resistances from 35bibliographies were considered.FHB resistance was evaluated infield or greenhouse conditions. Except for Jia and Chen(2005)who assessed FHB resistance following natural infection evaluations were conducted using artificial infection.Type II FHB resistance is evaluated by point inoculation. Type III resistance is identified by measuring the concentration of DON in the grain.Spray inocula-tion confounds Type I and Type II resistance.Type I resistance can be assessed by measuring disease incidence or comparing the results of spray and point inoculation(Rudd et al.2001;Miedaner et al. 2003).After projection,212QTLs remained for Meta-analysis.Nine original QTLs were discarded since they could not be projected onto the consensus map.QTLs-S(QTLs detected by spray inoculation or natural infection)mainly clustered on chromo-somes3B,5A and5B(Table3).Type II resistance QTLs were mainly located on chromosome3B (Table3).Six Type III resistance QTLs were pooled on3B;4on5A;2on1A,1B,2A and2D,and the remainder were scattered on the linkage map (Table3).Overall,the most FHB QTLs were projected onto chromosome3B, e.g.11QTLs-S from seven experiments,28Type II QTLs from16 experiments and six Type III QTLs from four experiments.PH QTL meta-analysisThere were generally at least two PH QTLs projected onto one chromosome.Thus,all the projected QTLs could be estimated by the software Meta-analysis. However,consensus QTLs could not be found on chromosomes1B,2B,3D,5D and7D.The results of PH QTL meta-analysis are listed in Table4.On each of chromosomes1D,2A,2D,3B,5B,6B and7B,just one meta-QTL(MQTL)was identified(P3,P4,P5, P9,P18,P22and P27).The MQTL P3containing three individual QTL positioned at60.5cM with a narrow C.I.of0.2cM.P4,P5,P18and P22 positioned at101.6,23.2,and127.7cM,aggregated two original QTLs from two experiments,respec-tively.Both P9and P27originated from initial QTLs of three experiments.Chromosomes1A,4A,4B,4D,5A,6D and7A had two MQTLs each.P12(4B)and P16(5A) integrated four individual QTLs.P13(4B)originated from three QTLs in three experiments.The other MQTLs were derived from two initial QTLs.QTLs from Araki et al.(1999),Cadalen et al. (1998)and Liu et al.(2002)could not be aggregated into an MQTL on chromosome3A.Every two of the remaining six projected QTLs were pooled into one group.MQTL P6,P7and P8were identified at position81.3(C.I.0.7cM),83.0(C.I.0.2cM),and 104.1cM(C.I.4.1cM),respectively.Most of the QTLs from eleven experiments were located on chromosome6A;these were classified into seven clusters and three MQTL were identified.P20, positioned at79.0cM on the composite map,was derived from eight PH QTLs detected in four experiments.P19and P21,located at34.9cM and 90.7cM,originated from two QTLs.FHB QTL meta-analysisThirty‘real’FHB QTLs occurred on13chromo-somes(Table5).Three MQTLs(F2,F3,F20)were on chromosome2D.Thefirst MQTL,F2,positioned at25.2cM,clustered the resistances from Wangshui-bai and Sumai 3.The second MQTL,F3,which integrated at68.6cM with a broad C.I.(14.1cM), originated from three QTLs from three experiments. The third MQTL,F20,sited at55.4cM,aggregated resistance QTLs from Wuhan-1and Sumai3.Most FHB QTLs(26studies)were located on chromosome3B.Among them,the most effective was from Sumai3.The others were from Wangshui-bai,Ning894037,Huapei57-2,Cj9306and Margin. The resistance QTLs-S grouped into six loci,two of which,positioned at14.4and24.7cM,aggregated three and two individual QTLs,respectively.Three ‘hot’positions of FHB QTL for Type II resistance, detected at14.3,17.2and46.3cM,derived from eight,ten and four initial QTLs,respectively.Three MQTLs(F28,F29and F30)for Type III resistance, were located at13.4,14.4and43.1cM,respectively, and each MQTL pooled two initial QTLs.On chromosome5A,four MQTLs were identified. The MQTLs-S(MQTLs derived from QTLs-S)F8 and F10,located at11.4and70.5cM,integrated three QTLs from three individual experiments.Both F9(MQTL-S)and F26(Type II FHB MQTL)derived from two initial loci.Three MQTLs(F14,F15and F27)were detected on chromosome6B.F14and F15, located at105.5and115.8cM,respectively,derivedfrom two QTLs-S,whereas F27,at118.8cM, aggregated three Type II QTLs from three experi-ments.On chromosome7AL,three consensus QTLs were found at127.9,137.8and165.4cM.The consensus loci F24and F25for Type II resistance were located on chromosome4D.F24, positioned at44.3cM,integrated three QTLs from two studies.F25integrated two QTLs and was located at112.5cM,with a broad C.I.of32.9cM, because the two initial QTLs were projected in a broad C.I.range(47.5,22.78cM).One MQTL was detected on each of chromosomes1B,2A,3A,4B, 5B,5D and6A.DiscussionRelationship between PH and FHBPH is controlled by Rht genes.In this study,thirty consensus QTLs on PH were identified.Five of them appeared to correspond to Rht genes:P5,to Rht8; P13,to Rht-B1(Rht1);P14,to Rht-D1(Rht2);P15, to Rht10;P16,to Rht9(Bo¨rner et al.1997;Cadalen et al.1998;Ellis et al.2005).Comparing the position and C.I.of PH and FHB consensus QTLs, coincidences were observed at several locations (Fig.1).Table4QTL meta-analysis results for plant heightMQTL Chr.a Positionof MQTL C.I.begin C.I.end Flanking markers C.I.R2(%)b No.ofprojectedQTLNo.ofstudiesP11A34.733.535.8XksuE18-Xwmc24 2.32422 P244.14444.1M77/P64-Xpsr3810.112.522 P31D60.560.460.6XcsEND2-Xfbb3770.29.532 P42A101.698.4104.8XksuF11-XWC0050pb 6.414.522 P52D23.220.725.7Xwmc431-Xwmc2556022 P63A81.380.981.6Xwmc388-Xcdo1180.73522 P78382.983.1Xcdo118-Xwmc2640.216.322 P8104.1102106.1Xcfa2134-Xfbb293 4.17.222 P93B20.419.821Xgwm493-Xcdo460 1.2943 P104A41.936.847Xrz574-Xgwm60110.211.922 P11105.3102.9107.8Xcdo780-Xcfd88 4.9–22 P124B313131Xgwm107-Xgwm66019.943 P133432.835.3Xgwm495-Xfba78 2.517.233 P144D44.142.545.6Xwmc419-Xwmc457338.822 P1534.029.338.7Xwmc473-Xcfd1939.536.722 P165A49.848.351.3Xpsr911-P31/M55-3 3.020.544 P1761.259.462.9P32/M51-XgbxG72210.511.822 P185B127.7126.1129.4P39/M49-135-Xbarc69 3.37.522 P196A34.933.935.9Xfba234-Xpsp3152 2.015.622 P207978.279.8Xbarc113-M60/P64.2 1.61384 P2190.787.893.6Xwmc417-Xfbb221 5.89.422 P226B160157.1162.9Xfba111-XWD124 5.87.922 P236D93.889.797.9Xcfd287-P43/M628.215.922 P24155.8153.1162.3P36/M61-Xfbb599.212.922 P257A91.178.8103.9P78/M49.4-Xbcd106625.110.622 P26163.7161.7165.7Xfba69-XgbxG411411.922 P277B47.746.249.2Xcdo595-Xfbb343 3.1 4.433a Chr.Chromosomeb R2mean R2of the MQTL;‘‘–’’R2of the QTL not documentedOur analysis revealed that consensus QTL P13 (Rht-B1)and FHB MQTL F7were linked at 35.3cM.Associations of Rht-B1and FHB reaction were reported in several studies(Hilton et al.1999; Steiner et al.2004;Srinivasachary et al.2009). Recently,Rht-B1was reported to be correlated with susceptibility to FHB under severe disease pressure, but under moderate pressure in thefield,Rht-B1had little effect on FHB reaction(Srinivasachary et al. 2009).On chromosome4D,MQTL Rht-D1(Rht2)and F24were located almost in the same region.The Rht-Table5QTL meta-analysis results of Fusarium head blight resistanceType of resistance MQTL Chr a Positionof MQTLC.I.begin C.I.end FlankingmarkersC.I.R(%)2Resistancesource cNumber ofprojectedQTLNumberof studiesMQTL-S F12A56.054.158.0Xgpw2225-Xgwm1223.98.7W,SP22F22D25.222.228.1Xgwm261-Xcdo1379 5.911.8S,W22F368.661.575.6Xgwm30-Xcfd23314.18.3S,A33F43A86.483.089.9Xwmc269-Xbcd22 6.912.1SP,FR22F53B14.41315.9Xbarc75-Xbarc147 2.910.4S,W33F624.723.825.6Xfbb185-Xbcd1278 1.89.1W22F74B36.335.337.3Xfba78-Xcdo1401213.1W22F85A11.410.812.0Xpsr644-Xbarc180 1.210.3W33F935.525.845.3Xcdo412-Xwg18419.511.6W,FR22F1070.569.771.3Xcdo1326-Xbarc319 1.614.7A,W22F115B51.450.752.1Xgwm213-Xwg889 1.410.5A,W33F125D75.474.876.0Xbarc322-Xwmc97 1.2 6.9R,W22F136A76.976.077.9P36/M47-Xfbb145 1.913.4SP,D22F146B105.5101.8109.1Xgwm644-XgbxG1387.311.2S22F15115.8111.8119.9Xbcd1299-XksuH148.1 6.7S,O22F167A127.9127.7128.1Xpsp3050-Xwmc1070.49.4SP,W22F17137.8132.0143.6Xwmc422-Xfba35411.610.0SP,A22F18165.4153.4177.5Xwmc426-Xwmc11624.19.5S,W22Type II F191B87.784.491.1Xfba178-Xbcd508 6.78.3A,W32 F202D55.45555.8Xfba341-Xwmc1490.810.9WH,S22F213B14.31414.6Xgwm533-XksuG530.631.6M,W,S,N87F2217.217.218.1Xcfd79-Xpsr567118.6H,W,S,N109F2346.344.847.9Xwmc471-Xfbb117315C,W44F244D44.343.545.1Xcfd71-Xfbb251 1.630.9SP,A32F25112.596128.9Xfbb322-Xwg11432.97SP,S22F265A37.235.538.9Xcdo412-Xgwm205 3.4 6.3S,W22F276B118.8118119.5M65/P64-Xpsr8 1.513.6A,S,W33Type III F283B13.413.113.8Xbarc75-Xfbb1560.713.9W22 F2914.413.914.8Xgwm533-XksuG530.98.6M,W22F3043.137.748.6Xgpw1120-P35/M6110.915.2C,W22a Chr.Chromosomeb R2mean R2of the MQTL;‘‘–’’R2of the QTL not documentedc S Sumai3,W Wangshuibai,A Arina,SP Spark,C CJ9306,M Margin,WH Wuhan-1,N Ning894037,O Opata85,H Huapei57-2, FR Frontana,R Renan,D DreamFig.1Maps of chromosomes2D,3A,4B,4D and7A with associated PH and FHB MQTL.Consistent MQTLs are shown in rectanglesD1effect on FHB was validated byfield trials (Draeger et al.2007;Srinivasachary et al.2008, 2009).Even under moderate disease pressure,the lines carrying Rht-D1displayed significantly higher FHB symptoms(Srinivasachary et al.2009).Both the PH and FHB MQTL are major QTLs,explaining 38.8%and30.9%of phenotypic variance in PH and FHB resistance,respectively.It is presumed that the genes are tightly linked,a single gene,or overlapping genes.In breeding programs comprising appropriate PH and FHB resistance,Rht-D1should be given more attention.P5(Rht8)co-localized with an FHB MQTL(F2) on chromosome2D.A negative relationship was reported by Miedaner and Voss(2008);over two years offield trials,Rht8increased FHB rating by 19%.On chromosome3A,FHB QTL F4and PH QTL P7partially overlapped.A coincidence of PH and FHB QTL on3A was not reported previously.Further study is required to confirm this association.MQTL P26and F18overlapped on chromosome 7A.The FHB MQTL was a minor QTL(R2,9.5%); therefore,the negative effect might be limited.This association was not reported previously.Coinci-dences of PH and FHB QTL were observed on chromosomes5A,5B and6A(Gervais et al.2003; Paillard et al.2004;Schmolke et al.2005).However, such results were not detected in the present meta-analysis.PH and FHB MQTLs on chromosomes5A and6A were adjacent,rather than co-located.The correlations between FHB resistance and PH are very complex.They might be due to morphological escape(Mesterha´zy1995,Buerstmayr et al.2000)or result from linkage or pleiotropy rather than an effect of height per se(Draeger et al.2007;Srinivasachary et al.2009).A similar negative relationship between Septoria nodorum blotch severity and PH was observed.Differences in leaf surface wetness(mainly dew)between short and tall genotypes were believed to be a major component of the pleiotropic mechanism (Scott et al.1985).Nevertheless,even if pleiotropy is involved,there must be other mechanisms involved in the effects of Rht1and Rht2on FHB reaction.There was no difference in relative humidity at ear height between tall and short lines with Rht1or Rht2(Hilton et al.1999).In other studies on the effects of Rht1and Rht2(Srinivasachary et al.2008,2009;Steiner et al. 2004;Draeger et al.2007),FHB reactions were evaluated in both thefield and greenhouse.In all these trials,humidity was artificially generated by misting or covering with cellophane bags.Gervais et al.(2003) conductedfield experiments with additional irrigation to homogenize the wetness of spikes,but dwarfing genotypes also showed more symptoms,so,such possible pleiotropy still cannot explain the association between FHB response and the PH gene on chromo-some5A.However,in thefield trials of Paillard et al. (2004)and Schmolke et al.(2005),no details were provided on humidity.Apparently,they did not apply irrigation in thefield experiments,but they also found a negative correlation between PH and FHB response, which resulted from either linkage between loci or pleiotropy.Sources of FHB resistanceAll the collated FHB QTLs were from16resistance sources.Sumai3and Wangshuibai were the main sources.Several resistant materials were derived from Sumai3,such as BW278,DH181and Ning 8026(Table2).FHB QTLs from different resistant sources were located in the same region.For exam-ple,F21was derived from the resistances from Sumai 3,Ning894037,Wangshuibai and Margin;F22was from Sumai3,Ning894037,Wangshuibai and Huapei 57-2.F27aggregated the resistances of Sumai3, Wangshuibai and Arina.The coincidences indicate that the different resistant sources contain the same FHB resistance,or that resistance genes are clustered in the consensus region.Resistance to FHB is neither pathogen species-or strain-specific(Van Eeuwijk et al.1995).Therefore,it is possible that the different sources might carry conservative or basal genes for resistance to FHB. Clustering of resistance genes(R genes)is common in plants(Michelmore and Meyers1998;Dangl and Jones2001;Smith et al.2007;Lin et al.2007).In wheat,R gene clusters have been reported for resistances to powdery mildew,leaf rust and stripe rust(Hu et al.2008;Chicaiza et al.2006).Dilbirligi et al.(2004)physically localized expressed R genes on wheat chromosomes and observedfive major R gene clusters spanning only*3%of the wheat genome.FHB resistances were differentiated into three main types based on different mechanisms(Schroe-der and Christensen1963).Several studies have revealed that some quantitative trait loci contributeto two or more types of resistance(Somers et al. 2003;Draeger et al.2007;Yu et al.2008b).In the current study,Type II(F21)and Type III(F28and F29)resistance MQTL,and MQTL-S(F5)were located at13.0–15.9cM on chromosome3B;and two MQTLs for Type II and Type III resistance overlapped at44.8–47.9cM on chromosome3B. Two coincident regions for Type I and Type II FHB QTLs were located on chromosomes5A and 6B.These results thus provide breeders with information for pyramiding different types of FHB resistance.ConclusionThe relationship between PH and FHB resistance was confirmed by QTL meta-analysis.Dwarfing genes differently affect FHB severity,and the mechanisms of the associations are complicated.Therefore,fur-ther studies of the relationships between different PH and FHB genes are required.Furthermore,the Rht effects should be carefully considered when selecting germplasm for improvement of FHB resistance. Some FHB MQTLs are common to several resistance sources.Investigation of these QTLs will help to reveal the mechanisms of FHB resistance.Four regions on chromosome3B,5A and6B are associ-ated with different types of FHB resistance.This information could be used for pyramiding genes for FHB resistances by marker assisted selection in wheat breeding programs.Acknowledgements We are grateful to Dr.Ji-Rui Wang and Dr.Peng-Fei Qi(Sichuan Agricultural University,China)for the review of the manuscript.This work was supported by the National Basic Research Program of China(973Program 2009CB118304)and the National High Technology Research and the Development Program of China(‘‘863’’Program 2006AA10Z179).ReferencesAhmed TA,Tsujimoto H,Sasakuma T(2000)QTLs associated with plant height and related characters in hexaploid wheat.Breed Sci50:267–273Anderson JA,Stack RW,Liu S,Waldron BL et al(2001)DNA markers for Fusarium head blight resistance QTLs in two wheat populations.Theor Appl Genet102:1164–1168 Appels R(2004)Wheat composite2004.da.gov/ggpages/map_shortlist.html Araki E,Miura H,Sawada S(1999)Identification of genetic loci affecting amylose content and agronomic traits on chromosome4A of wheat.Theor Appl Genet98:977–984Arcade A,Labourdette A,Falque M,Mangin B,Chardon F, Charcosset A,Joets J(2004)Biomercator:integrating genetic maps and QTL towards discovery of candidate genes.Bioinformatics20:2324–2326Arcade A,Labourdette A,Chardon F,Falque M,Charcosset A, Joets J(2005)BioMercator version2.1.http://generationcp.orgAyala L,Henry M,Ginkel M,Singh R,Keller B,Khairallah M (2002)Identification of QTLs for BYDV tolerance in bread wheat.Euphytica128:249–259Belknap JK,Atkins AL(2001)The replicability of QTL for murine alcohol preference drinking behavior across eight independent studies.Mamm Genome12:893–899Bo¨rner A,Ro¨der M,Korzun V(1997)Comparative molecular mapping of GA insensitive Rht loci on chromosomes4B and4D of common wheat(Triticum aestivum L.).Theor Appl Genet95:1133–1137Bo¨rner A,Schumann E,Fu¨rste A,Co¨ster H,Leithold B,Ro¨der MS,Weber WE(2002)Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat(Triticum aestivum L.).Theor Appl Genet105:921–936Bourdoncle W,Ohm HW(2003)Quantitative trait loci for resistance to Fusarium head blight in recombinant inbred wheat lines from the cross Huapei57–2/Patterson.Euphytica131:131–136Buerstmayr H,Steiner B,Lemmens M,Ruckenbauer P(2000) Resistance to Fusarium head blight in winter wheat:her-itability and trait associations.Crop Sci40:1012–1018Buerstmayr H,Lemmens M,Hartl L,Doldi L,Steiner B,Sti-erschneider M,Ruckenbauer P(2002)Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat.I.Resistance to fungal spread(Type II resistance).Theor Appl Genet104:84–91Cadalen T,Sourdille P,Charmet G,Tixier MH,Gay G,Boeuf C,Bernard S,Leroy P,Bernard M(1998)Molecular markers linked to genes affecting plant height in wheat using a doubled-haploid population.Theor Appl Genet 96:933–940Chardon F,Virlon B,Moreau L,Falque M,Joets J,Decousset L,Murigneux A,Charcosset A(2004)Genetic architec-ture offlowering time in maize as inferred from quanti-tative trait loci meta-analysis and synteny conservation with the rice genome.Genetics168:2169–2185 Chicaiza O,Khan IA,Zhang X,Brevis JC,Jackson L,Chen X, Dubcovsky J(2006)Registration offive wheat isogenic lines for leaf rust and stripe rust resistance genes.Crop Sci 46:485–487Cuthbert PA,Somers DJ,Thomas J,Cloutier S,Brule´-Babel A (2006)Fine mapping Fhb1a major gene controlling Fusarium head blight resistance in bread wheat(Triticum aestivum L.).Theor Appl Genet112:1465–1472 Cuthbert PA,Somers DJ,Brule´-Babel A(2007)Mapping of Fhb2on chromosome6BS:a gene controlling Fusarium head blightfield resistance in bread wheat(Triticum aestivum L.).Theor Appl Genet114:429–437。