{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T05:55:28Z","timestamp":1781502928706,"version":"3.54.1"},"reference-count":38,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T00:00:00Z","timestamp":1781481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007917","name":"Agricultural Research Service","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100007917","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:sec>\n                    <jats:title>Introduction<\/jats:title>\n                    <jats:p>\n                      Genomic studies in cacao (\n                      <jats:italic>Theobroma cacao<\/jats:italic>\n                      L.) have largely emphasized single-locus discovery, but less is known about whether repeated-harvest disease trajectories can be predicted from genome-wide markers to support long-term breeding objectives.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>We analyzed repeated-harvest phenotypes from 102 cacao accessions to derive longitudinal targets describing baseline performance and temporal change for healthy pod rate, frosty pod rot (FPR), and witches\u2019 broom disease (WBD). Genomic prediction was evaluated using random and relatedness-blocked cross-validation with single nucleotide polymorphism (SNP) marker sets aligned to the Criollo and Matina reference genomes. Robustness was assessed across trajectory model specifications, cross-validation block structures, and multi-trait selection indices.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Mixed-model analyses demonstrated temporal repeatability ranging from 0.78 to 0.89 across four harvests, with particularly high accession-level consistency for WBD traits. Genomic prediction models showed that WBD-derived targets, particularly branch and flower-cushion WBD symptom components, yielded more consistent predictive performance than FPR or healthy pod rate. These signals remained supported after 10,000-label permutation testing, Benjamini\u2013Hochberg false-discovery-rate correction, and multiple robustness analyses. Cross-reference comparisons indicated that WBD predictability was robust to the choice of reference genome, whereas other traits exhibited higher reference sensitivity. Finally, Pareto-based multi-trait prioritization identified a stable shortlist of candidate accessions optimizing both disease resilience and productivity.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Discussion<\/jats:title>\n                    <jats:p>Repeated-harvest disease phenotypes harbored reproducible accession-level temporal structure, with WBD-related longitudinal traits remaining genomically predictable across diverse validation settings. These findings indicate that repeated-harvest trajectory targets provide useful genomic-prediction endpoints for prioritizing resilient germplasm in perennial cacao breeding programs, while emphasizing the need for validation in larger multi-environment trials.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fpls.2026.1837102","type":"journal-article","created":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T05:37:29Z","timestamp":1781501849000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Longitudinal genomic prediction of cacao disease resilience identifies robust witches\u2019 broom disease targets"],"prefix":"10.3389","volume":"17","author":[{"given":"Insuck","family":"Baek","sequence":"first","affiliation":[{"name":"Environmental Microbial and Food Safety Laboratory, Agricultural Research Service, United States Department of Agriculture","place":["Beltsville, MD, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rakesh K.","family":"Upadhyay","sequence":"additional","affiliation":[{"name":"Department of Natural Sciences, College of Arts and Sciences, Bowie State University","place":["Bowie, MD, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moon S.","family":"Kim","sequence":"additional","affiliation":[{"name":"Environmental Microbial and Food Safety Laboratory, Agricultural Research Service, United States Department of Agriculture","place":["Beltsville, MD, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lyndel W.","family":"Meinhardt","sequence":"additional","affiliation":[{"name":"Sustainable Perennial Crops Laboratory, Agricultural Research Service, United States Department of Agriculture","place":["Beltsville, MD, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ezekiel","family":"Ahn","sequence":"additional","affiliation":[{"name":"Sustainable Perennial Crops Laboratory, Agricultural Research Service, United States Department of Agriculture","place":["Beltsville, MD, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,6,15]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1002\/tpg2.70069","article-title":"Machine learning-driven GWAS uncovers novel candidate genes for resistance to frosty pod rot and witches\u2019 broom disease in cacao","volume":"18","author":"Ahn","year":"2025","journal-title":"Plant Genome"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0228118","article-title":"Multi-trait random regression models increase genomic prediction accuracy for a temporal physiological trait derived from high-throughput phenotyping","volume":"15","author":"Baba","year":"2020","journal-title":"PloS One"},{"key":"B3","first-page":"409","article-title":"Cacao (Theobroma cacao L.) breeding","volume-title":"Advances in Plant Breeding Strategies: Industrial and Food Crops","author":"Bekele","year":"2019"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0260907","article-title":"Genome-wide association studies and genomic selection assays made in a large sample of cacao (Theobroma cacao L.) germplasm reveal significant marker-trait associations and good predictive value for improving yield potential","volume":"17","author":"Bekele","year":"2022","journal-title":"PloS One"},{"key":"B5","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1038\/hdy.2017.4","article-title":"Enhancing genomic prediction with genome-wide association studies in multiparental maize populations","volume":"118","author":"Bian","year":"2017","journal-title":"Heredity"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1002\/pld3.80","article-title":"Utilizing random regression models for genomic prediction of a longitudinal trait derived from high-throughput phenotyping","volume":"2","author":"Campbell","year":"2018","journal-title":"Plant Direct"},{"key":"B7","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1007\/s00122-014-2439-z","article-title":"Genomic selection prediction accuracy in a perennial crop: case study of oil palm (Elaeis guineensis Jacq.)","volume":"128","author":"Cros","year":"2015","journal-title":"Theor. Appl. Genet."},{"key":"B8","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1007\/s13593-024-00967-3","article-title":"Temporal behaviour of cacao clone production over 18 years","volume":"44","author":"Dessauw","year":"2024","journal-title":"Agron. Sustain. Dev."},{"key":"B9","doi-asserted-by":"publisher","first-page":"250","DOI":"10.3835\/plantgenome2011.08.0024","article-title":"Ridge regression and other kernels for genomic selection with R package rrBLUP","volume":"4","author":"Endelman","year":"2011","journal-title":"Plant Genome"},{"key":"B10","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1007\/978-3-319-24789-2_3","article-title":"Frosty pod rot (Moniliophthora roreri)","volume-title":"Cacao Diseases: A History of Old Enemies and New Encounters","author":"Evans","year":"2016"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1093\/g3journal\/jkae306","article-title":"Assessing genotype adaptability and stability in perennial forage breeding trials using random regression models for longitudinal dry matter yield data","volume":"15","author":"Fernandes Filho","year":"2025","journal-title":"G3: Genes Genomes Genet."},{"key":"B12","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1007\/s11032-022-01341-5","article-title":"Genomic selection for morphological and yield-related traits using genome-wide SNPs in oil palm","volume":"42","author":"Garz\u00f3n-Mart\u00ednez","year":"2022","journal-title":"Mol. Breed."},{"key":"B13","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1080\/0028825X.2003.9512860","article-title":"Witches\u2019 brooms and frosty pods: two major pathogens of cacao","volume":"41","author":"Griffith","year":"2003","journal-title":"N. Z. J. Bot."},{"key":"B14","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1080\/00401706.1970.10488634","article-title":"Ridge regression: biased estimation for nonorthogonal problems","volume":"12","author":"Hoerl","year":"1970","journal-title":"Technometrics"},{"key":"B15","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1007\/s11056-014-9422-z","article-title":"Genomic selection in forest tree breeding: the concept and an outlook to the future","volume":"45","author":"Isik","year":"2014","journal-title":"New For."},{"key":"B16","doi-asserted-by":"publisher","first-page":"2351","DOI":"10.1007\/s00122-015-2591-0","article-title":"Genomic approaches to selection in outcrossing perennials: focus on essential oil crops","volume":"128","author":"Kainer","year":"2015","journal-title":"Theor. Appl. Genet."},{"key":"B17","doi-asserted-by":"publisher","first-page":"963","DOI":"10.2307\/2529876","article-title":"Random-effects models for longitudinal data","volume":"38","author":"Laird","year":"1982","journal-title":"Biometrics"},{"key":"B18","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1007\/s12042-009-9038-1","article-title":"Infection biology of Moniliophthora perniciosa on Theobroma cacao and alternate solanaceous hosts","volume":"2","author":"Marelli","year":"2009","journal-title":"Trop. Plant Biol."},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.00343","article-title":"Prediction of cacao (Theobroma cacao) resistance to Moniliophthora spp. diseases via genome-wide association analysis and genomic selection","volume":"9","author":"McElroy","year":"2018","journal-title":"Front. Plant Sci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1819","DOI":"10.1093\/genetics\/157.4.1819","article-title":"Prediction of total genetic value using genome-wide dense marker maps","volume":"157","author":"Meuwissen","year":"2001","journal-title":"Genetics"},{"key":"B21","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1534\/genetics.120.303305","article-title":"Multi-trait genomic selection methods for crop improvement","volume":"215","author":"Moeinizade","year":"2020","journal-title":"Genetics"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.00681","article-title":"Integrating high-throughput phenotyping and statistical genomic methods to genetically improve longitudinal traits in crops","volume":"11","author":"Moreira","year":"2020","journal-title":"Front. Plant Sci."},{"key":"B23","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1186\/s12864-017-3920-2","article-title":"Genomic prediction in contrast to a genome-wide association study in explaining heritable variation of complex growth traits in breeding populations of Eucalyptus","volume":"18","author":"M\u00fcller","year":"2017","journal-title":"BMC Genomics"},{"key":"B24","doi-asserted-by":"publisher","first-page":"1713","DOI":"10.1534\/g3.120.401153","article-title":"Genome-wide association study reveals novel candidate genes associated with productivity and disease resistance to Moniliophthora spp. in cacao (Theobroma cacao L.)","volume":"10","author":"Osorio-Guar\u00edn","year":"2020","journal-title":"G3: Genes Genomes Genet."},{"key":"B25","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1111\/j.1365-3059.2007.01646.x","article-title":"Biodiversity and biogeography of the cacao (Theobroma cacao) pathogen Moniliophthora roreri in tropical America","volume":"56","author":"Phillips-Mora","year":"2007","journal-title":"Plant Pathol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"39","DOI":"10.2202\/1544-6115.1585","article-title":"Permutation p-values should never be zero: calculating exact p-values when permutations are randomly drawn","volume":"9","author":"Phipson","year":"2010","journal-title":"Stat. Appl. Genet. Mol. Biol."},{"key":"B27","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/978-3-319-24789-2_2","article-title":"The impact of diseases on cacao production: a global overview","volume-title":"Cacao Diseases: A History of Old Enemies and New Encounters","author":"Ploetz","year":"2016"},{"key":"B28","doi-asserted-by":"publisher","first-page":"904","DOI":"10.1038\/ng1847","article-title":"Principal components analysis corrects for stratification in genome-wide association studies","volume":"38","author":"Price","year":"2006","journal-title":"Nat. Genet."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1002\/tpg2.70058","article-title":"Accelerating perennial crop improvement via multi-omics-based predictive breeding","volume":"18","author":"Robinson","year":"2025","journal-title":"Plant Genome"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2017.01905","article-title":"Application of genome wide association and genomic prediction for improvement of cacao productivity and resistance to black and frosty pod diseases","volume":"8","author":"Romero Navarro","year":"2017","journal-title":"Front. Plant Sci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"2747","DOI":"10.1007\/s00122-022-04147-3","article-title":"Comparison of single-trait and multi-trait genomic predictions on agronomic and disease resistance traits in spring wheat","volume":"135","author":"Semagn","year":"2022","journal-title":"Theor. Appl. Genet."},{"key":"B32","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1007\/s11032-022-01326-4","article-title":"Genomic selection in tropical perennial crops and plantation trees: a review","volume":"42","author":"Seyum","year":"2022","journal-title":"Mol. Breed."},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1007\/s10681-019-2429-y","article-title":"Variation in yield over time in a cacao factorial mating design: changes in heritability and longitudinal data analyses over 13 consecutive years","volume":"215","author":"Tahi","year":"2019","journal-title":"Euphytica"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3390\/ani14202961","article-title":"Comparative study of single-trait and multi-trait genomic prediction models","volume":"14","author":"Tang","year":"2024","journal-title":"Animals"},{"key":"B35","doi-asserted-by":"publisher","first-page":"4414","DOI":"10.3168\/jds.2007-0980","article-title":"Efficient methods to compute genomic predictions","volume":"91","author":"VanRaden","year":"2008","journal-title":"J. Dairy Sci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1080\/01621459.1963.10500845","article-title":"Hierarchical grouping to optimize an objective function","volume":"58","author":"Ward","year":"1963","journal-title":"J. Am. Stat. Assoc."},{"key":"B37","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1111\/pbi.12848","article-title":"Cacao biotechnology: current status and future prospects","volume":"16","author":"Wickramasuriya","year":"2018","journal-title":"Plant Biotechnol. J."},{"key":"B38","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1186\/s12711-022-00724-8","article-title":"Application of Bayesian genomic prediction methods to genome-wide association analyses","volume":"54","author":"Wolc","year":"2022","journal-title":"Genet. Sel. Evol."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1837102\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,15]],"date-time":"2026-06-15T05:37:32Z","timestamp":1781501852000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2026.1837102\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,15]]},"references-count":38,"alternative-id":["10.3389\/fpls.2026.1837102"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2026.1837102","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,15]]},"article-number":"1837102"}}