Abstract
Yield is the most important and complex trait for genetic improvement in crops, and marker-assisted selection enhances the improvement efficiency. The USDA rice mini-core collection derived from over 18,000 accessions of global origins is an ideal panel for association mapping. We phenotyped 203 O. sativa accessions for 14 agronomic traits and identified 5 that were highly and significantly correlated with grain yield per plant: plant height, plant weight, tillers, panicle length, and kernels/branch. Genotyping with 155 genome-wide molecular markers demonstrated 5 main cluster groups. Linkage disequilibrium (LD) decayed at least 20 cM and marker pairs with significant LD ranged from 4.64 to 6.06% in four main groups. Model comparisons revealed that different dimensions of principal component analysis affected yield and its correlated traits for mapping accuracy, and kinship did not improve the mapping in this collection. Thirty marker–trait associations were highly significant, 4 for yield, 3 for plant height, 6 for plant weight, 9 for tillers, 5 for panicle length and 3 for kernels/branch. Twenty-one markers contributed to the 30 associations, because 8 markers were co-associated with 2 or more traits. Allelic analysis of OSR13, RM471 and RM7003 for their co-associations with yield traits demonstrated that allele 126 bp of RM471 and 108 bp of RM7003 should receive greater attention, because they had the greatest positive effect on yield traits. Tagging the QTLs responsible for multiple yield traits may simultaneously help dissect the complex yield traits and elevate the efficiency to improve grain yield using marker-assisted selection in rice.
Similar content being viewed by others
Abbreviations
- ARO:
-
Aromatic
- AUS:
-
Aus
- BIC:
-
Bayesian information criterion
- GSOR:
-
Genetic Stock Oryza
- IND:
-
Indica
- LD:
-
Linkage disequilibrium
- NJ:
-
Neighbor-Joining
- PCA:
-
Principal component analysis
- PCR:
-
Polymerase chain reaction
- PIC:
-
Polymorphic Information Content
- QTL:
-
Quantitative trait loci
- R 2 :
-
Squared allele frequency correlation estimates
- SNP:
-
Single nucleotide polymorphism
- SSR:
-
Simple sequence repeat
- TEJ:
-
Temperate japonica
- TRJ:
-
Tropical japonica
- UPGMA:
-
Unweighted pair-group method using arithmetic average
- URMC:
-
USDA rice mini-core collection
References
Abadie T, Cordeiro CMT, Fonseca JR, Alves RBN, Burle ML, Brondani C, Rangel PHN, Castro EM, Silva HT, Freire MS, Zimmermann FJP, Magalhaes JRSO (2005) Constructing a rice core collection for Brazil. Pesquisa Agropecu Bras 40:129–136
Abdurakhmonov IY, Abdukarimov A (2008) Application of association mapping to understanding the genetic diversity of plant germplasm. Int J Plant Genomics. doi:10.1155/2008/574927
Agrama HA, Eizenga GC (2008) Molecular diversity and genome-wide linkage disequilibrium patterns in a worldwide collection of Oryza sativa and its wild relatives. Euphytica 160:339–355
Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356
Agrama HA, Yan WG, Lee F, Fjellstrom R, Chen MH, Jia M, McClung A (2009) Genetic assessment of a mini-core subset developed from the USDA Rice Genebank. Crop Sci 49:1336–1346
Agrama HA, Yan WG, Jia M, Fjellstrom R, McClung A (2010) Genetic structure associated with diversity and geographic distribution in the USDA rice world collection. Nat Sci 2:247–291
Ando T, Yamamoto T, Shimizu T, Ma XF, Shomura A, Takeuchi Y, Lin SY, Yano M (2008) Genetic dissection and pyramiding of quantitative traits for panicle architecture by using chromosomal segment substitution lines in rice. Theor Appl Genet 116:881–890
Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C, Toomajian C, Traw B, Zheng H, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:531–539
Ashikari M, Wu J, Yano M, Sasaki T, Yoshimura A (1999) Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the alpha-subunit of GTP-binding protein. Proc Natl Acad Sci USA 96:10284–10289
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745
Bernardo R (2008) Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci 48:1649–1664
Borba TCO, Brondani RPV, Rangel PHN, Brondani C (2005) Evaluation of the number and information content of fluorescent-labeled SSR for rice germplasm characterization. Crop Breed Appl Biotechnol 2:157–165
Borba TCO, Brondani RPV, Rangel PHN, Brondani C (2009) Microsatellite marker-mediated analysis of the EMBRAPA Rice Core Collection genetic diversity. Genetica 137:293–304
Borba TCO, Brondani RPV, Breseghello F, Coelho ASG, Mendonça JA, Rangel PHN, Brondani C (2010) Association mapping for yield and grain quality traits in rice (Oryza sativa L.). Genet Mol Biol 33:515–524
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Brondani C, Rangel N, Brondani V, Ferreira E (2002) QTL mapping and introgression of yield-related traits from Oryza glumaepatula to cultivated rice (Oryza sativa) using microsatellite markers. Theor Appl Genet 104:1192–1203
Brondani C, Borba TCO, Rangel PHN, Brondani RPV (2006) Determination of traditional varieties of Brazilian rice using microsatellite markers. Genet Mol Biol 29:676–684
Brooks SA, Yan W, Jackson AK, Deren CW (2008) A natural mutation in rc reverts white-rice-pericarp to red and results in a new, dominant, wild-type allele:Rc-g. Theor Appl Genet 117:575–580
Chen Y, Lubberstedt T (2010) Molecular basis of trait correlations. Trends Plant Sci 15:454–461
Chu Y, Ramos L, Holbrook CC, Ozias-Akins P (2007) Frequency of a loss-of-function mutation in oleoyl-PC desaturase (ahFAD2A) in the mini-core of the U.S. peanut germplasm collection. Crop Sci 47:2372–2378
Cooper M, Podlich DW, Smith OS (2005) Gene-to-phenotype models and complex trait genetics. Aust J Agric Res 56:895–918
Devlin B, Roeder K (1999) Genomic control for association studies. Biometrics 55:997–1004
Devlin B, Bacanu SA, Roeder K (2004) Genomic control to the extreme. Nat Genet 36:1129–1130
Dhanraj A, Jagadish CA (1987) Studies on character association in the F2 generation of ten selected crosses in rice (Oryza sativa L.). J Res A FAU 15:64–65
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578
Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171
Farnir F, Coppieters W, Arranz J-J, Berzi P, Cambisano N, Grisart B, Karim L, Marcq F, Moreau L, Mni M, Nezer C, Simon P, Vanmanshoven P, Wagenaar D, Georges M (2000) Extensive genome-wide linkage disequilibrium in cattle. Genome Res 10:220–227
Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374
Flint-Garcia SA, Thuillet AC, Yu JM, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064
Franco J, Crossa J, Warburton ML, Taba S (2006) Sampling strategies for conserving maize diversity when forming core subsets using genetic markers. Crop Sci 46:854–864
Fu Q, Zhang P, Tan L, Zhu Z, Ma D, Fu Y, Zhan X, Cai H, Sun C (2010) Analysis of QTLs for yield-related traits in Yuanjiang common wild rice (Oryza rufipogon Griff.). J Genet Genomics 37:147–157
Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759–769
Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch SR (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638
Gravois KA, McNew RW (1993) Genetic relationships among and selection for rice yield and yield components. Crop Sci 33:249–252
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hemamalini GS, Shashidhar HE, Hittalmani S (2000) Molecular marker assisted tagging of morphological and physiological traits under two contrasting moisture regimes at peak vegetative stage in rice (Oryza sativa L.). Euphytica 112:69–78
Holbrook CC, Dong W (2005) Development and evaluation of a mini core collection for the U.S. peanut germplasm collection. Crop Sci 45:1540–1544
Holland J (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161
Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497
Hunter DJ, Kraft P, Jacobs KB, Cox DG, Yeager M, Hankinson SE, Wacholder S, Wang Z, Welch R, Hutchinson A, Wang J, Yu K, Chatterjee N, Orr N, Willett WC, Colditz GA, Ziegler RG, Berg CD, Buys SS, McCarty CA, Feigelson HS, Calle EE, Thun MJ, Hayes RB, Tucker M, Gerhard DS, Fraumeni JF Jr, Hoover RN, Thomas G, Chanock SJ (2007) A genome-wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer. Nat Genet 39:870–874
Huttley GA, Smit MW, Carrington HM, O’Brien SJ (1999) A scan for linkage disequilibrium across the human genome. Genetics 152:1711–1722
Inostroza L, Pozo AD, Matus I, Castillo D, Hayes P, Machado S, Corey A (2009) Association mapping of plant height, yield, and yield stability in recombinant chromosome substitution lines (RCSLs) using Hordeum vulgare subsp. spontaneum as a source of donor alleles in a Hordeum vulgare subsp. vulgare background. Mol Breed 23:365–376
Itoh H, Tatsumi T, Sakamoto T, Otomo K, Toyomasu T, Kitano H, Ashikari M, Ichihara S, Matsuoka M (2004) A rice semi-dwarf gene, Tan-Ginbozu (D35), encodes the gibberellin biosynthesis enzyme, ent-kaurene oxidase. Plant Mol Biol 54:533–547
Jiang GH, Xu CG, Li XH, He YQ (2004) Characterization of the genetic basis for yield and its component traits of rice revealed by doubled haploid population. Acta Genet Sinicavol 31:63–72
Jin L, Lu Y, Xiao P, Sun M, Corke H, Bao J (2010) Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 121:475–487
Kraakman ATW, Niks RE, Van den Berg PMMM, Stam P, Van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446
Li DJ, Sun CQ, Fu YC, Chen L, Zhu ZF, Li C, Cai HW, Wang XK (2002) Identification and mapping of genes for improving yield from Chinese common wild rice (O. rufipogon Griff.) using advanced backcross QTL analysis. Chin Sci Bull 18:1533–1537
Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621
Li C, Zhou A, Sang T (2006) Genetic analysis of rice domestication syndrome with the wild annual species, Oryza nivara. New Phytol 170:185–194
Li X, Yan W, Agrama H, Hu B, Jia L, Jia M, Jackson A, Moldenhauer K, McClung A, Wu D (2010) Genotypic and phenotypic characterization of genetic differentiation and diversity in the USDA rice mini-core collection. Genetica 138:1221–1230
Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129
Maccaferri M, Sanguineti MC, Noli E, Tuberosa R (2005) Population structure and long-range linkage disequilibrium in a drum wheat elite collection. Mol Breed 15:271–289
Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, Purugganan MD (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177:2223–2232
Moncada P, Martinez CP, Borrero J, Chatel M, Gauch H, Guimaraes E, Tohme J, McCouch SR (2001) Quantitative trait loci for yield and yield components in an Oryza sativa × Oryza rufipogon BC2F2 population evaluated in an upland environment. Theor Appl Genet 102:41–52
Nei M, Takezaki N (1983) Estimation of genetic distances and phylogenetic trees from DNA analysis. Proceedings of the 5th world congress. Genet Appl Livestock Prod 21:405–412
Novembre J, Stephens M (2008) Interpreting principal component analyses of spatial population genetic variation. Nat Genet 40:646–649
Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan D (2006) Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173:975–983
Pande S, Kishore GK, Upadhyaya HD, Rao JN (2006) Identification of sources of multiple disease resistance in mini-core collection of chickpea. Plant Dis 90:1214–1218
Patterson N, Price AL, Reich D (2007) Population structure and eigenanalysis. PLoS Genet 2:e90
Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rakshit S, Rakshit A, Matsumura H, Takahashi Y, Hasegawa Y, Ito A, Ishii T, Miyashita NT, Terauchi R (2007) Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114:731–743
Reich D, Price AL, Patterson N (2008) Principal component analysis of genetic data. Nat Genet 40:491–492
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Rohlf F (2000) NTSYS-PC numerical taxonomy and multivariate analysis system ver 2.11L. Applied Biostatistics, New York
Samonte SOP, Wilson LT, McClung AM (1998) Path analyses of yield and yield-related traits of fifteen diverse rice genotypes. Crop Sci 38:1130–1136
Shao Y, Jin L, Zhang G, Lu Y, Shen Y, Bao J (2010) Association mapping of grain color, phenolic content, flavonoid content and antioxidant capacity in dehulled rice. Theor Appl Genet. doi:10.1007/s00122-010-1505-4
Sharma RS, Choubey SD (1985) Correlation studies in upland rice. Indian J Agron 30:87–88
Sharma R, Rao VP, Upadhyaya HD, Reddy VG, Thakur RP (2010) Resistance to grain mold and downy mildew in a mini-core collection of sorghum germplasm. Plant Dis 94:439–444
Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182:851–861
Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630
Spielmeyer W, Ellis MH, Peter M (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048
Stich B, Melchinger AE, Frisch M, Maurer HP, Heckenberger M, Reif JC (2005) Linkage disequilibrium in European elite maize germplasm investigated with SSRs. Theor Appl Genet 111:723–730
Stich B, Maurer HP, Melchinger AE, Frisch M, Heckenberger M, van der Voort JR, Peleman J, Sørensen AP, Reif JC (2006) Comparison of linkage disequilibrium in elite European maize inbred lines using AFLP and SSR markers. Mol Breed 17:217–226
Stich B, Möhring J, Piepho HP, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754
Suh JP, Ahn SN, Cho YC, Kang KH, Choi IS, Kim YG, Suh HS, Hong HC (2005) Mapping of QTLs for yield traits using an advanced backcross population from a cross between Oryza sativa and O. glaberrima. Korean J Breed 37:214–220
Sweeney MT, Thomson MJ, Pfeil BE, McCouch S (2006) Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18:283–294
Takahashi Y, Shomura A, Sasaki T, Yano M (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA 98:7922–7927
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Terao T, Nagata K, Morino K, Hirose T (2010) A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor Appl Genet 120:875–893
Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinea CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107:479–493
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Upadhyaya HD (2005) Variability for drought resistance related traits in the mini core collection of peanut. Crop Sci 45:1432–1440
Upadhyaya HD, Oritz R (2001) A mini-core collection for capturing diversity and promoting utilization of chickpea genetic resources in crop improvement. Theor Appl Genet 102:1292–1298
Upadhyaya HD, Reddy LJ, Gowda CLL, Reddy KN, Singh S (2006) Development of a mini core for enhanced and diversified utilization of pigeonpea germplasm resources. Crop Sci 46:2127–2132
Upadhyaya HD, Pundir RPS, Dwivedi SL, Gowda CLL, Reddy VG, Singh S (2009) Developing a mini core collection of sorghum for diversified utilization of germplasm. Crop Sci 49:1769–1780
Wang ML, Zhu C, Barkley NA, Chen Z, Erpelding JE, Murray SC, Tuinstra MR, Tesso T, Pederson GA, Yu J (2009) Genetic diversity and population structure analysis of accessions in the US historic sweet sorghum collection. Theor Appl Genet 120:13–23
Weir BS (1996) Genetic data analysis. II. Methods for discrete population genetic data. Sinauer Associates, Sunderland
Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447:661–678
Xin Z, Velten JP, Oliver MJ, Burke JJ (2003) Highthroughput DNA extraction method suitable for PCR. Biotechniques 34:820–826
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 143:1–7
Yan WG, Rutger JN, Bockelman HE, Tai TH (2005a) Agronomic evaluation and seed stock establishment of the USDA rice core collection. In Norman RJ et al (eds) B.R. Wells rice research studies 2004. University of Arkansas, Agricultural Experiment Station Research Series 529, pp 63–68
Yan WG, Rutger JN, Bockelman HE, Tai TH (2005b) Evaluation of kernel characteristics of the USDA rice core collection. In Norman RJ et al (eds) B.R. Wells rice research studies 2004. University of Arkansas, Agricultural Experiment Station Research Series 529, pp 69–74
Yan WG, Rutger JN, Bryant RJ, Bockelman HE, Fjellstrom RG, Chen MH, Tai TH, McClung AM (2007) Development and evaluation of a core subset of the USDA rice (Oryza sativa L.) germplasm collection. Crop Sci 47:869–878
Yan WG, Li Y, Agrama HA, Luo D, Gao F, Lu X, Ren G (2009) Association mapping of stigma and spikelet characteristics in rice (Oryza sativa L.). Mol Breed 24:277–292
Yeager M, Orr N, Hayes RB, Jacobs KB, Kraft P, Wacholder S, Minichiello MJ, Fearnhead P, Yu K, Chatterjee N, Wang Z, Welch R, Staats BJ, Calle EE, Feigelson HS, Thun MJ, Rodriguez C, Albanes D, Virtamo J, Weinstein S, Schumacher FR, Giovannucci E, Willett WC, Cancel-Tassin G, Cussenot O, Valeri A, Andriole GL, Gelmann EP, Tucker M, Gerhard DS, Fraumeni JF Jr, Hoover R, Hunter DJ, Chanock SJ, Thomas G (2007) Genome-wide association study of prostate cancer identifies a second risk locus at 8q24. Nat Genet 39:645–649
Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhu C, Yu J (2009) Nonmetric multidimensional scaling corrects for population structure in association mapping with different sample types. Genetics 182:875–888
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, X., Yan, W., Agrama, H. et al. Mapping QTLs for improving grain yield using the USDA rice mini-core collection. Planta 234, 347–361 (2011). https://doi.org/10.1007/s00425-011-1405-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-011-1405-0