{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T19:58:33Z","timestamp":1787687913294,"version":"build-2784847793"},"reference-count":41,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2022,5,27]],"date-time":"2022-05-27T00:00:00Z","timestamp":1653609600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000981","name":"Hort Innovation","doi-asserted-by":"publisher","award":["AP19003"],"award-info":[{"award-number":["AP19003"]}],"id":[{"id":"10.13039\/501100000981","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000981","name":"Hort Innovation","doi-asserted-by":"publisher","award":["RCM 6472"],"award-info":[{"award-number":["RCM 6472"]}],"id":[{"id":"10.13039\/501100000981","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Agriculture Victoria","award":["AP19003"],"award-info":[{"award-number":["AP19003"]}]},{"name":"Agriculture Victoria","award":["RCM 6472"],"award-info":[{"award-number":["RCM 6472"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The triggers of biennial bearing are thought to coincide with embryonic development in apple and occurs within the first 70 days after full bloom (DAFB). Strong evidence suggests hormonal signals are perceived by vegetative apple spur buds to induce flowering. The hormonal response is typically referred to as the floral induction (FI) phase in bud meristem development. To determine the metabolic pathways activated in FI, young trees of the biennial bearing cultivar \u2018Nicoter\u2019 and the less susceptible cultivar \u2018Rosy Glow\u2019 were forced into an alternate cropping cycle over five years and an inverse relationship of crop load and return bloom was established. Buds were collected over a four-week duration within 70 DAFB from trees that had maintained a four-year biennial bearing cycle. Metabolomics profiling was undertaken to determine the differentially expressed pathways and key signalling molecules associated with biennial bearing. Marked metabolic differences were observed in trees with high and low crop load treatments. Significant effects were detected in members of the phenylpropanoid pathway comprising hydroxycinnamates, salicylates, salicylic acid biosynthetic pathway intermediates and flavanols. This study identifies plant hormones associated with FI in apples using functional metabolomics analysis.<\/jats:p>","DOI":"10.3390\/ijms23116019","type":"journal-article","created":{"date-parts":[[2022,5,27]],"date-time":"2022-05-27T07:05:07Z","timestamp":1653635107000},"page":"6019","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Metabolic Pathways for Observed Impacts of Crop Load on Floral Induction in Apple"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1504-1126","authenticated-orcid":false,"given":"Priyanka","family":"Reddy","sequence":"first","affiliation":[{"name":"Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, VIC 3083, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6826-2689","authenticated-orcid":false,"given":"Tim","family":"Plozza","sequence":"additional","affiliation":[{"name":"Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, VIC 3083, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vilnis","family":"Ezernieks","sequence":"additional","affiliation":[{"name":"Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, VIC 3083, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8656-3490","authenticated-orcid":false,"given":"Dario","family":"Stefanelli","sequence":"additional","affiliation":[{"name":"Manjimup Horticulture Research Centre, Department of Primary Industries and Regional Development, Manjimup, WA 6258, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6224-0411","authenticated-orcid":false,"given":"Alessio","family":"Scalisi","sequence":"additional","affiliation":[{"name":"Tatura SmartFarm, Agriculture Victoria, Tatura, VIC 3616, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ian","family":"Goodwin","sequence":"additional","affiliation":[{"name":"Tatura SmartFarm, Agriculture Victoria, Tatura, VIC 3616, Australia"},{"name":"Centre for Agricultural Innovation, University of Melbourne, Parkville, VIC 3010, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8442-6081","authenticated-orcid":false,"given":"Simone","family":"Rochfort","sequence":"additional","affiliation":[{"name":"Agriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, VIC 3083, Australia"},{"name":"School of Applied Systems Biology, La Trobe University, Bundoora, VIC 3083, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Korban, S.S. (2021). Economic importance of the world apple industry. The Apple Genome, Springer International Publishing.","DOI":"10.1007\/978-3-030-74682-7"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1002\/9781118060773.ch5","article-title":"Alternate bearing in fruit trees","volume":"4","author":"Monselise","year":"1982","journal-title":"Hortic. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1093\/jxb\/err261","article-title":"Genetic control of biennial bearing in apple","volume":"63","author":"Guitton","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1622","DOI":"10.21273\/HORTSCI.42.7.1622","article-title":"Effect of blossom density and crop load on growth, fruit quality, and return bloom in \u2018Honeycrisp\u2019 apple","volume":"42","author":"Embree","year":"2007","journal-title":"HortScience"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1080\/15538362.2021.1951922","article-title":"Effects of different crop loads on physiological, yield and fruit quality of \u2018JoyaTM\u2019 apple trees: High crop load decreases maximum daily trunk diameter and does not affect stem water potential","volume":"21","author":"Atay","year":"2021","journal-title":"Int. J. Fruit Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"286","DOI":"10.3389\/fpls.2021.604810","article-title":"Toward systematic understanding of flower bud induction in apple: A multi-omics approach","volume":"12","author":"Milyaev","year":"2021","journal-title":"Front. Plant Sci."},{"key":"ref_7","unstructured":"Arseneault, M.H. (2016). Crop Load Management of Apple by Chemical Fruitlet Thinning, Preharvest Drop Management, and Investigation of Abscission Physiology. [Ph.D. Thesis, University of Guelph]."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.3389\/fpls.2020.01213","article-title":"Relationships among the rootstock, crop load, and sugar hormone signaling of apple tree, and their effects on biennial bearing","volume":"11","author":"Kviklys","year":"2020","journal-title":"Front. Plant Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/BF00390146","article-title":"The induction of flowering in vitro in stem segments of Plumbago indica L.\u2014I. The production of vegetative buds","volume":"72","author":"Nitsch","year":"1967","journal-title":"Planta"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1007\/BF00390147","article-title":"The induction of flowering in vitro in stem segments of Plumbago indica L.\u2014II. The production of reproductive buds","volume":"72","author":"Nitsch","year":"1967","journal-title":"Planta"},{"key":"ref_11","first-page":"1","article-title":"No flower no fruit\u2014Genetic potentials to trigger flowering in fruit trees","volume":"1","author":"Hanke","year":"2007","journal-title":"Genes Genomes Genom."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"317","DOI":"10.21273\/HORTTECH.9.3.317","article-title":"Physiological factors affecting biennial bearing in tree fruit: The role of seeds in apple","volume":"9","author":"Dennis","year":"1999","journal-title":"HortTechnology"},{"key":"ref_13","unstructured":"Harley, C.P., Magness, J., Masure, M., Fletcher, L., and Degman, E. (1942). Investigations on the Cause and Control of Biennial Bearing of Apple Trees."},{"key":"ref_14","first-page":"409","article-title":"Gibberellins and cytokinins related to fruit bud initiation in apple","volume":"636","author":"Benavides","year":"2004","journal-title":"Acta Hortic."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"93","DOI":"10.17660\/ActaHortic.1978.80.14","article-title":"The role of seed derived hormones in the control of flowering in apple","volume":"80","author":"Hoad","year":"1978","journal-title":"Acta Hortic."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Guitton, B., Kelner, J.-J., Celton, J.-M., Sabau, X., Renou, J.-P., Chagn\u00e9, D., and Costes, E. (2016). Analysis of transcripts differentially expressed between fruited and deflowered \u2018Gala\u2019adult trees: A contribution to biennial bearing understanding in apple. BMC Plant Biol., 16.","DOI":"10.1186\/s12870-016-0739-y"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1897","DOI":"10.1007\/s13361-016-1469-y","article-title":"Untargeted metabolomics strategies\u2014Challenges and emerging directions","volume":"27","author":"Codreanu","year":"2016","journal-title":"J. Am. Soc. Mass Spectrom."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s11306-007-0082-2","article-title":"Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI)","volume":"3","author":"Sumner","year":"2007","journal-title":"Metabolomics"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1007\/s10535-015-0581-3","article-title":"Effect of crop load on phytohormones, sugars, and biennial bearing in apple trees","volume":"60","author":"Sirtautas","year":"2016","journal-title":"Biol. Plant."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Ram\u00edrez, H. (2021, May 24). Endogenous Cytokinins and Fruit Bud Formation in Apple. pp. 245\u2013248. Available online: https:\/\/www.actahort.org\/books\/514\/514_28.htm.","DOI":"10.17660\/ActaHortic.2000.514.28"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e0156","DOI":"10.1199\/tab.0156","article-title":"Salicylic acid biosynthesis and metabolism","volume":"9","author":"Dempsey","year":"2011","journal-title":"Arab. Book"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"53","DOI":"10.3389\/fenvs.2014.00053","article-title":"Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants","volume":"2","author":"Das","year":"2014","journal-title":"Front. Environ. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1104\/pp.106.082040","article-title":"Production and scavenging of reactive oxygen species in chloroplasts and their functions","volume":"141","author":"Asada","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1784","DOI":"10.1104\/pp.103.032185","article-title":"The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1","volume":"134","author":"Barth","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/0092-8674(94)90544-4","article-title":"H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response","volume":"79","author":"Levine","year":"1994","journal-title":"Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S1360-1385(96)80048-3","article-title":"Mannitol metabolism in plants: A method for coping with stress","volume":"1","author":"Stoop","year":"1996","journal-title":"Trends Plant Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.1104\/pp.100.3.1541","article-title":"Role of salicylic acid and benzoic acid in flowering of a photoperiod-insensitive strain, lemna paucicostata LP6","volume":"100","author":"Khurana","year":"1992","journal-title":"Plant Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1093\/oxfordjournals.pcp.a076954","article-title":"The role of benzoic acid and plant hormones in flowering of Lemna gibba G3","volume":"26","author":"Fujioka","year":"1985","journal-title":"Plant Cell Physiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.plantsci.2013.07.004","article-title":"Redox control of plant growth and development","volume":"211","author":"Kocsy","year":"2013","journal-title":"Plant Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"15762","DOI":"10.1038\/s41598-020-72895-7","article-title":"Differential expression of genes in olive leaves and buds of ON- versus OFF-crop trees","volume":"10","author":"Dastkar","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1078\/0176-1617-01041","article-title":"The metabolic pathway of salicylic acid rather than of chlorogenic acid is involved in the stress-induced flowering of Pharbitis nil","volume":"160","author":"Hatayama","year":"2003","journal-title":"J. Plant Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"944","DOI":"10.4161\/psb.5.8.11826","article-title":"Stress-induced flowering","volume":"5","author":"Wada","year":"2010","journal-title":"Plant Signal. Behav."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1046\/j.1365-313X.2003.01954.x","article-title":"Salicylic acid regulates flowering time and links defence responses and reproductive development","volume":"37","author":"Pons","year":"2004","journal-title":"Plant J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1111\/j.1365-313X.2007.03359.x","article-title":"The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure","volume":"53","author":"Jin","year":"2008","journal-title":"Plant J."},{"key":"ref_35","first-page":"1465","article-title":"Induction of flowering in lemna paucicostata by dicoumarol and 4-hydroxycoumarin","volume":"26","author":"Kaihara","year":"1985","journal-title":"Plant Cell Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1266\/ggs.77.383","article-title":"His-Asp phosphorelay signal transduction in higher plants: Receptors and response regulators for cytokinin signaling in Arabidopsis thaliana","volume":"77","author":"Oka","year":"2002","journal-title":"Genes Genet. Syst."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1023\/A:1005954525087","article-title":"The involvement of cytokinins in plant responses to environmental stress","volume":"23","author":"Hare","year":"1997","journal-title":"Plant Growth Regul."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1309","DOI":"10.21273\/HORTSCI.39.6.1309","article-title":"Blossom and fruitlet thinners affect crop load, fruit weight, seed number, and return bloom of \u2018Northern Spy\u2019 apple","volume":"39","author":"Nichols","year":"2004","journal-title":"HortScience"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2450","DOI":"10.1093\/jxb\/eraa590","article-title":"Alternate bearing in fruit trees: Fruit presence induces polar auxin transport in citrus and olive stem and represses IAA release from the bud","volume":"72","author":"Haim","year":"2021","journal-title":"J. Exp. Bot."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"487B-487","DOI":"10.21273\/HORTSCI.35.3.487B","article-title":"532 Endogenous Gibberellins in Developing Apple Seeds in Relation to Biennial Bearing","volume":"35","author":"Tu","year":"2000","journal-title":"HortScience"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"W251","DOI":"10.1093\/nar\/gkv380","article-title":"MetaboAnalyst 3.0-making metabolomics more meaningful","volume":"43","author":"Xia","year":"2015","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/11\/6019\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:19:37Z","timestamp":1760138377000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/11\/6019"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,27]]},"references-count":41,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2022,6]]}},"alternative-id":["ijms23116019"],"URL":"https:\/\/doi.org\/10.3390\/ijms23116019","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,27]]}}}