Genome-wide association study for in vitro digestibility and related traits in triticale forage.

Forage GWAS QTL SNP Triticale in vitro digestibility

Journal

BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807

Informations de publication

Date de publication:
27 Mar 2024
Historique:
received: 31 10 2023
accepted: 19 03 2024
medline: 28 3 2024
pubmed: 28 3 2024
entrez: 28 3 2024
Statut: epublish

Résumé

Triticale is making its way on dairy farms as an alternative forage crop. This requires the availability of high-yielding triticale varieties with good digestibility. Triticale forage breeding mainly focussed on biomass yield, but efforts to improve digestibility are increasing. We previously investigated the interrelationships among different quality traits in soft dough triticale: starch, acid detergent fibre and in vitro digestibility of organic matter (IVOMD) and of neutral detergent fibre (IVNDFD) of the total plant, IVNDFD and Klason lignin of the stems, and ear proportion and stem length. Here we determine the genetic control of these traits, using a genome-wide association (GWAS) approach. A total of 33,231 DArTseq SNP markers assessed in a collection of 118 winter triticale genotypes, including 101 varieties and 17 breeding lines, were used. The GWAS identified a total of 53 significant marker-trait associations (MTAs). The highest number of significantly associated SNP markers (n = 10) was identified for total plant IVNDFD. A SNP marker on chromosome 1A (4211801_19_C/T; 474,437,796 bp) was found to be significantly associated with ear proportion, and plant and stem IVNDFD, with the largest phenotypic variation for ear proportion (R² A collection of 118 winter triticale genotypes combined with DArTseq SNP markers served as a source for identifying 53 MTAs and several candidate genes for forage IVD and related traits through a GWAS approach. Taken together, the results of this study demonstrate that the genetic diversity available in this collection can be further exploited for research and breeding purposes to improve the IVD of triticale forage.

Sections du résumé

BACKGROUND BACKGROUND
Triticale is making its way on dairy farms as an alternative forage crop. This requires the availability of high-yielding triticale varieties with good digestibility. Triticale forage breeding mainly focussed on biomass yield, but efforts to improve digestibility are increasing. We previously investigated the interrelationships among different quality traits in soft dough triticale: starch, acid detergent fibre and in vitro digestibility of organic matter (IVOMD) and of neutral detergent fibre (IVNDFD) of the total plant, IVNDFD and Klason lignin of the stems, and ear proportion and stem length. Here we determine the genetic control of these traits, using a genome-wide association (GWAS) approach. A total of 33,231 DArTseq SNP markers assessed in a collection of 118 winter triticale genotypes, including 101 varieties and 17 breeding lines, were used.
RESULTS RESULTS
The GWAS identified a total of 53 significant marker-trait associations (MTAs). The highest number of significantly associated SNP markers (n = 10) was identified for total plant IVNDFD. A SNP marker on chromosome 1A (4211801_19_C/T; 474,437,796 bp) was found to be significantly associated with ear proportion, and plant and stem IVNDFD, with the largest phenotypic variation for ear proportion (R²
CONCLUSIONS CONCLUSIONS
A collection of 118 winter triticale genotypes combined with DArTseq SNP markers served as a source for identifying 53 MTAs and several candidate genes for forage IVD and related traits through a GWAS approach. Taken together, the results of this study demonstrate that the genetic diversity available in this collection can be further exploited for research and breeding purposes to improve the IVD of triticale forage.

Identifiants

pubmed: 38539072
doi: 10.1186/s12870-024-04927-7
pii: 10.1186/s12870-024-04927-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

223

Subventions

Organisme : Fachagentur Nachwachsende Rohstoffe
ID : 22024515
Organisme : Horizon 2020
ID : 101000847

Informations de copyright

© 2024. The Author(s).

Références

Mergoum M, Sapkota S, ElDoliefy AEA, Naraghi SM, Pirseyedi S, Alamri MS, et al. Triticale (x Triticosecale Wittmack) breeding. In: Al-Khayri J, Jain S, Johnson D, editors. Adv Plant Breed Strateg cereal. Cham: Springer, Switzerland;; 2019. pp. 405–51.
doi: 10.1007/978-3-030-23108-8_11
Oettler G. The fortune of a botanical curiosity - Triticale: past, present and future. J Agric Sci. 2005;143:329–46.
doi: 10.1017/S0021859605005290
McGoverin CM, Snyders F, Muller N, Botes W, Fox G, Manley M. A review of triticale uses and the effect of growth environment on grain quality. J Sci Food Agric. 2011;91:1155–65.
pubmed: 21433010 doi: 10.1002/jsfa.4338
Ayalew H, Kumssa TT, Butler TJ, Ma XF. Triticale improvement for forage and cover crop uses in the Southern Great Plains of the United States. Front Plant Sci. 2018;9:1–9.
doi: 10.3389/fpls.2018.01130
Baron VS, Juskiw PE, Aljarrah M. Triticale as a forage. In: Eudes F, editor. Triticale. Cham: Springer; 2015. pp. 189–212.
doi: 10.1007/978-3-319-22551-7_10
Mergoum M, Gómez-Macpherson H. Triticale improvement and production. Volume 179. Rome: Food and Agriculture Organization of the United Nations; 2004.
Nielsen DC, Vigil MF, Benjamin JG. Forage yield response to water use for dryland corn, millet, and triticale in the Central Great Plains. Agron J. 2006;98:992–8.
doi: 10.2134/agronj2005.0356
Cao D, Wang D, Li S, Li Y, Hao M, Liu B. Genotyping-by-sequencing and genome-wide association study reveal genetic diversity and loci controlling agronomic traits in triticale. Theor Appl Genet. 2022;135:1705–15.
pubmed: 35244733 doi: 10.1007/s00122-022-04064-5
Faccini N, Morcia C, Terzi V, Rizza F, Badeck F-W. Triticale Italy Biology (Basel). 2023;12:1308.
pubmed: 37887018
Saha MC, Baker JL, Bouton JH. Registration of ‘NF201’ forage triticale. J Plant Regist. 2015;9:185–9.
doi: 10.3198/jpr2014.10.0078crc
Swanckaert J. Assessing plant type and the nutritive value of silage maize in the perspective of the Belgian official variety trials, PhD thesis. Ghent University; 2016.
Aljarrah M, Oatway L, Albers S, Bergen C. Variability, heritability and genetic advance in some agronomic and forage quality characters of spring triticale in western Canada. Commun Agric Appl Biol Sci. 2014;79:9–18.
pubmed: 26072570
Aljarrah M, Capettini F, Lohr S, Oatway L. Triticale production and utilization in Western Canada, evaluation triticale lines for grain and forage yield and quality [Conference presentation]. 10th International Triticale Symposium 2019, Lethbridge, Canada, 15–19 July, 2019; 2019.
Linn JG, Martin NP. Forage quality analyses and interpretation. Vet Clin North Am Food Anim Pract. 1991;7:509–23.
pubmed: 1654176 doi: 10.1016/S0749-0720(15)30790-8
Forejtová J, Lád F, Třinaáctý J, Richter M, Gruber L, Doležal P, et al. Comparison of organic matter digestibility determined by in vivo and in vitro methods. Czech J Anim Sci. 2005;50:47–53.
doi: 10.17221/3994-CJAS
Barrière Y, Guillet C, Goffner D, Pichon M. Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review. Anim Res. 2003;52:193–228.
doi: 10.1051/animres:2003018
Chaves AV, Waghorn GC, Tavendale MH. A simplified method for lignin measurement in a range of forage species. Proc New Zeal Grassl Assoc. 2002;129–33.
Jung HJG, Samac DA, Sarath G. Modifying crops to increase cell wall digestibility. Plant Sci. 2012;185–186:65–77.
pubmed: 22325867 doi: 10.1016/j.plantsci.2011.10.014
Bilgili U, Cifci EA, Hanoglu H, Yagdi K, Acikgoz E. Yield and quality of triticale forage. J Food Agric Environ. 2009;7:556–60.
Haesaert G, Derycke V, Latré J, Debersaque F, D’hooghe K, Coomans D, et al. A study on triticale (× Triticosecale Wittmack) for whole plant silage in Belgium. In: Arseniuk E, Osiński R, editors. Proc 5th int Triticale Symp Radzików, Poland, 30 June – 5 July, 2002. Plant Breeding and Acclimatization Institute, Radzików, Poland; 2002. pp. 261–9.
Lekgari LA, Baenziger PS, Vogel KP, Baltensperger DD. Identifying winter forage triticale (×Triticosecale wittmack) strains for the central Great Plains. Crop Sci. 2008;48:2040–8.
doi: 10.2135/cropsci2008.01.0048
Manni K, Lötjönen T, Huuskonen A. Comparing spring triticale varieties to barley and wheat varieties when harvested as whole crop. Agric Food Sci. 2021;30:24–35.
doi: 10.23986/afsci.100693
Cherney JH, Marten GC. Small grain crop forage potential: II. Interrelationships among biological, chemical, morphological, and anatomical determinants of quality. Crop Sci. 1982;22:240–5.
doi: 10.2135/cropsci1982.0011183X002200020010x
Fohner G. Harvesting maximum value from small grain cereal forages. Proc West Alfalfa Forage Conf. 2002;52–7.
Méchin V, Argillier O, Menanteau V, Barrière Y, Mila I, Pollet B, et al. Relationship of cell wall composition to in vitro cell wall digestibility of maize inbred line stems. J Sci Food Agric. 2000;80:574–80.
doi: 10.1002/(SICI)1097-0010(200004)80:5<574::AID-JSFA575>3.0.CO;2-R
van Parijs F. Cell wall digestibility of perennial ryegrass: an association mapping approach, PhD thesis. Ghent University; 2016.
Barrière Y, Laperche A, Barrot L, Aurel G, Briand M, Jouanin L. QTL analysis of lignification and cell wall digestibility in the Bay-0 x Shahdara RIL progeny of Arabidopsis thaliana as a model system for forage plant. Plant Sci. 2005;168:1235–45.
doi: 10.1016/j.plantsci.2005.01.001
Méchin V, Argillier O, Hébert Y, Guingo E, Moreau L, Charcosset A, et al. Genetic analysis and QTL mapping of cell wall digestibility and lignification in silage maize. Crop Sci. 2001;41:690–7.
doi: 10.2135/cropsci2001.413690x
Cardinal AJ, Lee M, Moore KJ. Genetic mapping and analysis of quantitative trait loci affecting fiber and lignin content in maize. Theor Appl Genet. 2003;106:866–74.
pubmed: 12647061 doi: 10.1007/s00122-002-1136-5
Krakowsky MD, Lee M, Coors JG. Quantitative trait loci for cell-wall components in recombinant inbred lines of maize (Zea mays L.) I: stalk tissue. Theor Appl Genet. 2005;111:337–46.
pubmed: 15902397 doi: 10.1007/s00122-005-2026-4
Krakowsky MD, Lee M, Coors JG. Quantitative trait loci for cell wall components in recombinant inbred lines of maize (Zea mays L.) II: Leaf sheath tissue. Theor Appl Genet. 2006;112:717–26.
pubmed: 16362276 doi: 10.1007/s00122-005-0175-0
Li K, Wang H, Hu X, Liu Z, Wu Y, Huang C. Genome-wide association study reveals the genetic basis of stalk cell wall components in maize. PLoS ONE. 2016;11.
Vinayan MT, Babu R, Jyothsna T, Zaidi PH, Blümmel M. A note on potential candidate genomic regions with implications for maize stover fodder quality. F Crop Res. 2013;153:102–6.
doi: 10.1016/j.fcr.2013.03.018
Wang H, Li K, Hu X, Liu Z, Wu Y, Huang C. Genome-wide association analysis of forage quality in maize mature stalk. BMC Plant Biol. 2016;16:1–12.
doi: 10.1186/s12870-016-0919-9
Li K, Wang H, Hu X, Ma F, Wu Y, Wang Q, et al. Genetic and quantitative trait locus analysis of cell wall components and forage digestibility in the zheng58 × HD568 maize RIL population at anthesis stage. Front Plant Sci. 2017;8:1–10.
Lorenzana RE, Lewis MF, Jung HJG, Bernardo R. Quantitative trait loci and trait correlations for maize stover cell wall composition and glucose release for cellulosic ethanol. Crop Sci. 2010;50:541–55.
doi: 10.2135/cropsci2009.04.0182
Murray SC, Rooney WL, Mitchell SE, Sharma A, Klein PE, Mullet JE, et al. Genetic improvement of sorghum as a biofuel feedstock: II. QTL for stem and leaf structural carbohydrates. Crop Sci. 2008;48:2180–93.
doi: 10.2135/cropsci2008.01.0068
Shiringani AL, Friedt W. QTL for fibre-related traits in grain × sweet sorghum as a tool for the enhancement of sorghum as a biomass crop. Theor Appl Genet. 2011;123:999–1011.
pubmed: 21739141 doi: 10.1007/s00122-011-1642-4
Joshi AK, Kumar U, Mishra VK, Chand R, Chatrath R, Naik R, et al. Variations in straw fodder quality and grain–straw relationships in a mapping population of 287 diverse spring wheat lines. F Crop Res. 2019;243:107627.
doi: 10.1016/j.fcr.2019.107627
Li J, Tang W, Zhang YW, Chen KN, Wang C, Liu Y, et al. Genome-wide association studies for five forage quality-related traits in sorghum (Sorghum bicolor L). Front Plant Sci. 2018;9:1–8.
Neuweiler JE, Maurer HP, Würschum T. Long-term trends and genetic architecture of seed characteristics, grain yield and correlated agronomic traits in triticale (×Triticosecale Wittmack). Plant Breed. 2020;139:717–29.
doi: 10.1111/pbr.12821
Neuweiler JE, Maurer HP, Würschum T. Genetic architecture of phenotypic indices for simultaneous improvement of protein content and grain yield in triticale (×Triticosecale). Plant Breed. 2021;140:232–45.
doi: 10.1111/pbr.12894
Trini J, Maurer HP, Neuweiler JE, Würschum T. Identification and fine-mapping of quantitative trait loci controlling plant height in central European winter triticale (× Triticosecale wittmack). Plants. 2021;10.
De Zutter A, De Boever J, Muylle H, Roldán-Ruiz I, Haesaert G. In vitro digestibility as screening tool for improved forage quality in triticale. F Crop Res. 2023;301:article109009.
doi: 10.1016/j.fcr.2023.109009
De Zutter A. Genotypic and phenotypic diversity of triticale in relation to cell wall digestibility, PhD thesis. Ghent University, Belgium; 2023.
Zadoks JC, Chang TT, Konzak CF. A decimal code for the growth stages of cereals. Weed Res. 1974;14:415–21.
doi: 10.1111/j.1365-3180.1974.tb01084.x
De Zutter A, Landschoot S, Vermeir P, Van Waes C, Muylle H, Roldán-Ruiz I et al. Variation in potential feeding value of triticale forage among plant fraction, maturity stage, growing season and genotype. Heliyon. 2023;9:article e12760.
R Development Core Team. R: A language and environment for statistical computing (version 4.2.0), Foundation for Statistical Computing, Vienna, Australia. https://www.r-project.org/ ; 2022.
Piepho HP, Möhring J, Melchinger AE, Büchse A. BLUP for phenotypic selection in plant breeding and variety testing. Euphytica. 2008;161:209–28.
doi: 10.1007/s10681-007-9449-8
Gruber B, Unmack PJ, Berry OF, Georges A. DARTR: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Mol Ecol Resour. 2018;18:691–9.
pubmed: 29266847 doi: 10.1111/1755-0998.12745
Schwender H, Ickstadt K. Imputing missing genotypes with weighted k nearest. J Toxicol Environ Health. 2012;75:438–46.
doi: 10.1080/15287394.2012.674910
Schwender H, Fritsch A, Scrime. : Analysis of high-dimensional categorical data such as SNP data (version 1.3.5). https://cran.r-project.org/web/packages/scrime/index.html ; 2018.
Jombart T, Ahmed I. Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. 2011;27:3070–1.
Murtagh F, Legendre P. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion ? J Classif. 2014;295:274–95.
doi: 10.1007/s00357-014-9161-z
Wang J, Zhang Z. GAPIT version 3: boosting power and accuracy for genomic. Genomics Proteom Bioinf. 2021;19:629–40.
doi: 10.1016/j.gpb.2021.08.005
Hill WG, Weir BS. Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol. 1988;33:54–78.
pubmed: 3376052 doi: 10.1016/0040-5809(88)90004-4
Delourme R, Falentin C, Fomeju BF, Boillot M, Lassalle G, André I, et al. High-density SNP-based genetic map development and linkage disequilibrium assessment in Brassica napus L. BMC Genomics. 2013;14:1–18.
doi: 10.1186/1471-2164-14-120
Li X, Han Y, Wei Y, Acharya A, Farmer AD, Ho J et al. Development of an alfalfa SNP array and its use to evaluate patterns of population structure and linkage disequilibrium. PLoS ONE. 2014;9.
Yao E, Blake VC, Cooper L, Wight CP, Michel S, Cagirici HB et al. GrainGenes: a data-rich repository for small grains genetics and genomics. Database. 2022;2022.
Blake VC, Birkett C, Matthews DE, Hane DL, Bradbury P, Jannink J. The Triticeae Toolbox: combining phenotype and genotype data to advance small-grains breeding. Plant Genome. 2016;9.
Galiano-Carneiro AL, Boeven PHG, Maurer HP, Würschum T, Miedaner T. Genome-wide association study for an efficient selection of Fusarium head blight resistance in winter triticale. Euphytica. 2019;215.
Losert D, Maurer HP, Marulanda JJ, Würschum T. Phenotypic and genotypic analyses of diversity and breeding progress in European triticale (× Triticosecale Wittmack). Plant Breed. 2017;136:18–27.
doi: 10.1111/pbr.12433
Niedziela A, Orłowska R, Machczyńska J, Bednarek PT. The genetic diversity of triticale genotypes involved in Polish breeding programs. Springerplus. 2016;5:355.
pubmed: 27066368 pmcid: 4801839 doi: 10.1186/s40064-016-1997-8
Ayalew H, Anderson JD, Krom N, Tang Y, Butler TJ, Tiwari V et al. Genotyping-by-sequencing and genomic selection applications in hexaploid triticale. G3 Genes, Genomes, Genet. 2022;12.
Ma X-F, Fang P, Gustafson JP. Polyploidization-induced genome variation in triticale. Genome. 2004;47:839–48.
pubmed: 15499398 doi: 10.1139/g04-051
Ma XF, Gustafson JP. Allopolyploidization-accommodated genomic sequence changes in triticale. Ann Bot. 2008;101:825–32.
pubmed: 18252766 pmcid: 2710212 doi: 10.1093/aob/mcm331
Lei L, Goltsman E, Goodstein D, Wu GA, Rokhsar DS, Vogel JP. Plant pan-genomics comes of age. Annu Rev Plant Biol. 2021;72:411–35.
pubmed: 33848428 doi: 10.1146/annurev-arplant-080720-105454
Tams SH, Bauer E, Oettler G, Melchinger AE. Genetic diversity in European winter triticale determined with SSR markers and coancestry coefficient. Theor Appl Genet. 2004;108:1385–91.
pubmed: 14760487 doi: 10.1007/s00122-003-1552-1
Tams SH, Melchinger AE, Bauer E. Genetic similarity among European winter triticale elite germplasms assessed with AFLP and comparisons with SSR and pedigree data. Plant Breed. 2005;124:154–60.
doi: 10.1111/j.1439-0523.2004.01047.x
Ammar K, Mergoum M, Rajaram S. The history and evolution of triticale. In: Mergoum M, Gómez-Macpherson H, editors. Triticale Improv prod. 179th ed. Rome: Food and Agriculture Organization of the United Nations; 2004. pp. 1–10.
Zillinsky FJ. The development of triticale. Adv Agron. 1974;26:315–48.
doi: 10.1016/S0065-2113(08)60875-5
Ittu G, Săulescu NN. Triticale breeding in Fundulea-Romania. In: Guedes-Pinto H, Darvey N, Carnide VP, editors. Triticale today tomorrow dev plant breeding. Volume 5. Dordrecht: Springer; 1996. pp. 663–8.
doi: 10.1007/978-94-009-0329-6_86
Neuweiler JE, Trini J, Maurer HP, Würschum T. Do lower nitrogen fertilization levels require breeding of different types of cultivars in triticale? Theor Appl Genet. 2022;135:993–1009.
pubmed: 34958397 doi: 10.1007/s00122-021-04012-9
Long AD, Langley CH. The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res. 1999;9:720–31.
pubmed: 10447507 pmcid: 310800 doi: 10.1101/gr.9.8.720
Boerjan W, Ralph J, Baucher M. Lignin biosynthesis. Annu Rev Plant Biol. 2003;54:519–46.
pubmed: 14503002 doi: 10.1146/annurev.arplant.54.031902.134938
Vermaas JV, Dixon RA, Chen F, Mansfield SD, Boerjan W, Ralph J, et al. Passive membrane transport of lignin-related compounds. Proc Natl Acad Sci U S A. 2019;116:23117–23.
pubmed: 31659054 pmcid: 6859372 doi: 10.1073/pnas.1904643116
Do THT, Martinoia E, Lee Y. Functions of ABC transporters in plant growth and development. Curr Opin Plant Biol. 2018;41:32–8.
pubmed: 28854397 doi: 10.1016/j.pbi.2017.08.003
Zhang L, Xing J, Lin J. At the intersection of exocytosis and endocytosis in plants. New Phytol. 2019;224:1479–89.
pubmed: 31230354 doi: 10.1111/nph.16018
Chebli Y, Bidhendi AJ, Kapoor K, Geitmann A. Cytoskeletal regulation of primary plant cell wall assembly. Curr Biol. 2021;31:R681–95.
pubmed: 34033798 doi: 10.1016/j.cub.2021.03.092
Komis G, Luptovciak I, Doskocilova A, Samaj J. Biotechnological aspects of cytoskeletal regulation in plants. Biotechnol Adv. 2015;33:1043–62.
pubmed: 25784147 doi: 10.1016/j.biotechadv.2015.03.008
Wyman C, Decker S, Himmel M, Brady J, Skopec C, Viikari L. Hydrolysis of cellulose and hemicellulose. Polysaccharides. 2004.
Yeats TH, Bacic A, Johnson KL. Plant Glycosylphosphatidylinositol anchored proteins at the plasma membrane-cell wall nexus. J Integr Plant Biol. 2018;60:649–69.
pubmed: 29667761 doi: 10.1111/jipb.12659
Du Y, Fu X, Chu Y, Wu P, Liu Y, Ma L et al. Biosynthesis and the roles of plant sterols in development and stress responses. Int J Mol Sci. 2022;23.
Jones DM, Murray CM, Ketelaar KJ, Thomas JJ, Villalobos JA, Wallace IS. The emerging role of protein phosphorylation as a critical regulatory mechanism controlling cellulose biosynthesis. Front Plant Sci. 2016;7:1–12.
doi: 10.3389/fpls.2016.00684
Schrick K, Fujioka S, Takatsuto S, Stierhof YD, Stransky H, Yoshida S, et al. A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J. 2004;38:227–43.
pubmed: 15078327 doi: 10.1111/j.1365-313X.2004.02039.x
Vogel J. Unique aspects of the grass cell wall. Curr Opin Plant Biol. 2008;11:301–7.
pubmed: 18434239 doi: 10.1016/j.pbi.2008.03.002
Pauly M, Keegstra K. Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu Rev Plant Biol. 2016;67:235–59.
pubmed: 26927904 doi: 10.1146/annurev-arplant-043015-112222
Rocha JRDASDC, Marçal TDS, Salvador FV, Da Silva AC, Carneiro PCS, De Resende MDV, et al. Unraveling candidate genes underlying biomass digestibility in elephant grass (Cenchrus purpureus). BMC Plant Biol. 2019;19:1–12.
doi: 10.1186/s12870-019-2180-5

Auteurs

Anneleen De Zutter (A)

Faculty of Bioscience Engineering, Department of Plants and Crops, Ghent University, Diepestraat 1, Bottelare, 9820, Belgium. anneleen.dezutter@ugent.be.

Maria Chiara Piro (MC)

Faculty of Bioscience Engineering, Department of Plants and Crops, Ghent University, Diepestraat 1, Bottelare, 9820, Belgium.

Steven Maenhout (S)

Faculty of Bioscience Engineering, Department of Plants and Crops, Ghent University, Coupure Links 653, Ghent, 9000, Belgium.

Hans Peter Maurer (HP)

State Plant Breeding Institute, University of Hohenheim, 70599, Stuttgart, Germany.

Johan De Boever (J)

Animal Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Scheldeweg 68, Melle, 9090, Belgium.

Hilde Muylle (H)

Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Caritasstraat 39, Melle, 9090, Belgium.

Isabel Roldán-Ruiz (I)

Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Caritasstraat 39, Melle, 9090, Belgium.

Geert Haesaert (G)

Faculty of Bioscience Engineering, Department of Plants and Crops, Ghent University, Diepestraat 1, Bottelare, 9820, Belgium.

Classifications MeSH