{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T16:11:19Z","timestamp":1787069479437,"version":"build-2736575974"},"reference-count":105,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2025,3,26]],"date-time":"2025-03-26T00:00:00Z","timestamp":1742947200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"publisher","award":["310030_185251"],"award-info":[{"award-number":["310030_185251"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Yunnan Innovation Team Project","award":["202305AS350004"],"award-info":[{"award-number":["202305AS350004"]}]},{"DOI":"10.13039\/501100018538","name":"Ten-thousand Talents Program","doi-asserted-by":"crossref","award":["YNWR-QNBJ-2018-318"],"award-info":[{"award-number":["YNWR-QNBJ-2018-318"]}],"id":[{"id":"10.13039\/501100018538","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["U23A20149"],"award-info":[{"award-number":["U23A20149"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Second Tibetan Plateau Scientific Expedition and Research Program","award":["2019QZKK0502"],"award-info":[{"award-number":["2019QZKK0502"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,5,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The frost resistance of new foliage and flowers and their relationship with the phenology of leaf-out and flowering are essential for explaining plant species distribution in seasonally cold climates. In this study, we performed a congeneric, elevational comparison of phenology with frost resistance in evergreen Rhododendron species in the Southeastern Himalayas. A comparison of the microclimate with long-term meteorological records of low temperature extremes permitted the calculation of a realistic, long-term margin of safety for 12 Rhododendron species. Surprisingly, frost resistance and phenological events were matching for leaf-out time (not flowering) in higher elevation species only. Flower-leaf sequence (FLS) and frost resistance were linked for species at higher elevation and the earliest flowering species at lower elevation only. Despite a selection of FLS by elevation, flowers (including petals, filaments and ovaries) were still prone to frost damage during the early growing season at both lower and higher elevations, while new leaves were generally safe on long-term scales, regardless of phenology and elevation. In contrast to lower montane elevation, where severe frost is rare in spring, treeline elevation species maintain safety margins over centennial time-scales by adjusting leaf-out phenology. Our data show an evolutionary priority of leaf survival over flower survival. Both, physiological acclimation and phylogenetic components contribute to these adjustments. Rare extreme frost events restrict the upper range limit of the examined Rhododendron species by affecting new foliage. It is essential to know the actual temperature extremes at organ level rather than relying on weather station records.<\/jats:p>","DOI":"10.1093\/treephys\/tpaf036","type":"journal-article","created":{"date-parts":[[2025,3,23]],"date-time":"2025-03-23T06:47:25Z","timestamp":1742712445000},"source":"Crossref","is-referenced-by-count":3,"title":["How phenology interacts with frost tolerance in Southeastern Himalayan\n                    <i>Rhododendron<\/i>\n                    species"],"prefix":"10.1093","volume":"45","author":[{"given":"Hongyan","family":"Jin","sequence":"first","affiliation":[{"name":"Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences , Lanhei Road 132, Kunming, Yunnan 650201 ,","place":["PR China"]},{"name":"University of Chinese Academy of Sciences , Yanqihu East Road 1, Huairou District, Beijing 101408 ,","place":["PR China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoqing","family":"Yin","sequence":"additional","affiliation":[{"name":"Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences , Lanhei Road 132, Kunming, Yunnan 650201 ,","place":["PR China"]},{"name":"University of Chinese Academy of Sciences , Yanqihu East Road 1, Huairou District, Beijing 101408 ,","place":["PR China"]},{"name":"School of Life Sciences, Yunnan University , Huannan Road, East of University Town, Chenggong New Area, Kunming 650500 ,","place":["PR China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yue","family":"Qi","sequence":"additional","affiliation":[{"name":"Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences , Lanhei Road 132, Kunming, Yunnan 650201 ,","place":["PR China"]},{"name":"University of Chinese Academy of Sciences , Yanqihu East Road 1, Huairou District, Beijing 101408 ,","place":["PR China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jurriaan M","family":"de Vos","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences (Botany), University of Basel , Sch\u00f6nbeinstrasse 6, Basel 4056 ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hang","family":"Sun","sequence":"additional","affiliation":[{"name":"Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences , Lanhei Road 132, Kunming, Yunnan 650201 ,","place":["PR China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"K\u00f6rner","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences (Botany), University of Basel , Sch\u00f6nbeinstrasse 6, Basel 4056 ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Yang","sequence":"additional","affiliation":[{"name":"Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences , Lanhei Road 132, Kunming, Yunnan 650201 ,","place":["PR China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,3,26]]},"reference":[{"key":"2025053009565013400_ref1","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1080\/02827581.2012.663403","article-title":"Inheritance of height growth and autumn cold hardiness based on two generations of full-sib and half-sib families of","volume":"27","author":"Abrahamsson","year":"2012","journal-title":"Scand J For Res"},{"key":"2025053009565013400_ref2","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1111\/j.1365-2435.2009.01587.x","article-title":"Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest","volume":"23","author":"Augspurger","year":"2009","journal-title":"Funct Ecol"},{"key":"2025053009565013400_ref3","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1093\/treephys\/tpn045","article-title":"Temporal variation of nonstructural carbohydrates in montane conifers: similarities and differences among developmental stages, species and environmental conditions","volume":"29","author":"Bansal","year":"2009","journal-title":"Tree Physiol"},{"key":"2025053009565013400_ref4","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1093\/treephys\/tpu021","article-title":"Photoperiod and temperature responses of bud swelling and bud burst in four temperate forest tree species","volume":"34","author":"Basler","year":"2014","journal-title":"Tree Physiol"},{"key":"2025053009565013400_ref5","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1007\/s12229-021-09273-z","article-title":"A comprehensive review on the taxonomy, ecology, reproductive biology, economic importance and conservation status of Indian Himalayan rhododendrons","volume":"88","author":"Basnett","year":"2022","journal-title":"Bot Rev"},{"key":"2025053009565013400_ref6","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1007\/s00035-019-00225-3","article-title":"Floral traits determine pollinator visitation in Rhododendron species across an elevation gradient in the Sikkim Himalaya","volume":"129","author":"Basnett","year":"2019","journal-title":"Alp Bot"},{"key":"2025053009565013400_ref7","doi-asserted-by":"publisher","first-page":"717","DOI":"10.1111\/j.0014-3820.2003.tb00285.x","article-title":"Testing for phylogenetic signal in comparative data: behavioral traits are more labile","volume":"57","author":"Blomberg","year":"2003","journal-title":"Evolution"},{"key":"2025053009565013400_ref8","doi-asserted-by":"publisher","first-page":"e1003537","DOI":"10.1371\/journal.pcbi.1003537","article-title":"BEAST 2: a software platform for Bayesian evolutionary analysis","volume":"10","author":"Bouckaert","year":"2014","journal-title":"PLoS Comput Biol"},{"key":"2025053009565013400_ref9","doi-asserted-by":"publisher","first-page":"2922","DOI":"10.1111\/1365-2745.13708","article-title":"Differences between flower and leaf phenological responses to environmental variation drive shifts in spring phenological sequences of temperate woody plants","volume":"109","author":"Buonaiuto","year":"2021","journal-title":"J Ecol"},{"key":"2025053009565013400_ref10","doi-asserted-by":"publisher","first-page":"1206","DOI":"10.1111\/nph.16848","article-title":"Reconciling competing hypotheses regarding flower-leaf sequences in temperate forests for fundamental and global change biology","volume":"229","author":"Buonaiuto","year":"2021","journal-title":"New Phytol"},{"key":"2025053009565013400_ref11","doi-asserted-by":"publisher","first-page":"2312","DOI":"10.1111\/nph.19685","article-title":"Ecological drivers of flower-leaf sequences: aridity and proxies for pollinator attraction select for flowering-first in the American plums","volume":"242","author":"Buonaiuto","year":"2024","journal-title":"New Phytol"},{"key":"2025053009565013400_ref12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v080.i01","article-title":"Brms: an R package for Bayesian multilevel models using Stan","volume":"80","author":"B\u00fcrkner","year":"2017","journal-title":"J Stat Softw"},{"key":"2025053009565013400_ref13","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1002\/j.1477-8696.1997.tb06268.x","article-title":"Spring phenology of trees and frost avoidance","volume":"52","author":"Cannell","year":"1997","journal-title":"Weather"},{"key":"2025053009565013400_ref14","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1111\/1365-2745.12482","article-title":"Frost sensitivity of leaves and flowers of subalpine plants is related to tissue type and phenology","volume":"104","author":"Caradonna","year":"2016","journal-title":"J Ecol"},{"key":"2025053009565013400_ref15","doi-asserted-by":"publisher","first-page":"3149","DOI":"10.1098\/rstb.2010.0142","article-title":"Why does phenology drive species distribution?","volume":"365","author":"Chuine","year":"2010","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"2025053009565013400_ref16","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1046\/j.1461-0248.2001.00261.x","article-title":"Phenology is a major determinant of tree species range","volume":"4","author":"Chuine","year":"2008","journal-title":"Ecol Lett"},{"key":"2025053009565013400_ref17","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1111\/j.1095-8339.1978.tb02361.x","article-title":"Rhododendron seed from the Palaeocene of southern England","volume":"76","author":"Collinson","year":"1978","journal-title":"Bot J Linn Soc"},{"key":"2025053009565013400_ref18","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1126\/science.abb4484","article-title":"Ancient orogenic and monsoon-driven assembly of the world's richest temperate alpine flora","volume":"369","author":"Ding","year":"2020","journal-title":"Science"},{"key":"2025053009565013400_ref19","doi-asserted-by":"publisher","first-page":"1771","DOI":"10.1002\/ajb2.1174","article-title":"Phenological sequences: how early-season events define those that follow","volume":"105","author":"Ettinger","year":"2018","journal-title":"Am J Bot"},{"key":"2025053009565013400_ref20","volume-title":"Reports of the agro-ecological zones project. World soil resources report 48 vol. 1: Methodology and results for Africa; vol. 2: South-West Asia; vol. 3: South and central America; vol. 4: South-East Asia","author":"FAO","year":"1978\u20131981"},{"key":"2025053009565013400_ref21","first-page":"110","article-title":"Altitudinal patterns of plant species diversity and community structure on Yulong Mountains, Yunnan","volume":"24","author":"Feng","year":"2006","journal-title":"China J Mt Sci"},{"key":"2025053009565013400_ref22","doi-asserted-by":"publisher","first-page":"229","DOI":"10.4141\/cjps67-043","article-title":"Index of injury\u2014a useful expression of freezing injury to plant tissues as determined by the electrolytic method","volume":"47","author":"Flint","year":"1967","journal-title":"Can J Plant Sci"},{"key":"2025053009565013400_ref23","doi-asserted-by":"publisher","first-page":"3101","DOI":"10.1098\/rstb.2010.0145","article-title":"Toward a synthetic understanding of the role of phenology in ecology and evolution","volume":"365","author":"Forrest","year":"2010","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"2025053009565013400_ref24","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1890\/02-0651","article-title":"A comparative demography of plants based upon elasticities of vital rates","volume":"85","author":"Franco","year":"2004","journal-title":"Ecology"},{"key":"2025053009565013400_ref25","doi-asserted-by":"publisher","first-page":"404","DOI":"10.1111\/1755-0998.13479","article-title":"Testing genome skimming for species discrimination in the large and taxonomically difficult genus Rhododendron","volume":"22","author":"Fu","year":"2022","journal-title":"Mol Ecol Resour"},{"key":"2025053009565013400_ref26","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1111\/nph.15270","article-title":"Sequence of flower and leaf emergence in deciduous trees is linked to ecological traits, phylogenetics, and climate","volume":"220","author":"Gougherty","year":"2018","journal-title":"New Phytol"},{"key":"2025053009565013400_ref27","doi-asserted-by":"publisher","first-page":"3338","DOI":"10.1016\/j.cub.2023.06.064","article-title":"Climatic drivers and ecological implications of variation in the time interval between leaf-out and flowering","volume":"33","author":"Guo","year":"2023","journal-title":"Curr Biol"},{"key":"2025053009565013400_ref28","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.plantsci.2010.07.013","article-title":"Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling","volume":"180","author":"Hacker","year":"2011","journal-title":"Plant Sci"},{"key":"2025053009565013400_ref29","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1046\/j.1525-142x.2000.00003e.x","article-title":"Evo-devo or devo-evo \u2014 does it matter","volume":"2","author":"Hall","year":"2000","journal-title":"Evol Dev"},{"key":"2025053009565013400_ref30","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1111\/j.1365-3040.1991.tb01514.x","article-title":"Does climatic warming increase the risk of frost damage in northern trees?","volume":"14","author":"H\u00e4nninen","year":"1991","journal-title":"Plant Cell Environ"},{"key":"2025053009565013400_ref31","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.ppees.2018.09.001","article-title":"Vulnerability of phenological progressions over season and elevation to climate change: rhododendrons of Mt","volume":"34","author":"Hart","year":"2018","journal-title":"Yulong Perspect Plant Ecol Evol Syst"},{"key":"2025053009565013400_ref32","doi-asserted-by":"publisher","first-page":"10615","DOI":"10.1073\/pnas.1403376111","article-title":"Herbarium specimens show contrasting phenological responses to Himalayan climate","volume":"111","author":"Hart","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025053009565013400_ref33","doi-asserted-by":"publisher","first-page":"198","DOI":"10.3732\/ajb.1500440","article-title":"Fast and cheap in the fall: phylogenetic determinants of late flowering phenologies in Himalayan Rhododendron","volume":"103","author":"Hart","year":"2016","journal-title":"Am J Bot"},{"key":"2025053009565013400_ref34","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1071\/bt9800587","article-title":"Frost resistance of subalpine eucalyptus species. I. Experiments using a radiation frost room","volume":"28","author":"Harwood","year":"1980","journal-title":"Aust J Bot"},{"key":"2025053009565013400_ref35","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1111\/jbi.12171","article-title":"Community phylogenetics at the biogeographical scale: cold tolerance, niche conservatism and the structure of north American forests","volume":"41","author":"Hawkins","year":"2014","journal-title":"J Biogeogr"},{"key":"2025053009565013400_ref36","doi-asserted-by":"publisher","first-page":"2365","DOI":"10.1111\/j.1365-2486.2012.02712.x","article-title":"Ecological impacts of a widespread frost event following early spring leaf-out","volume":"18","author":"Hufkens","year":"2012","journal-title":"Glob Chang Biol"},{"key":"2025053009565013400_ref37","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1046\/j.1461-0248.2000.00165.x","article-title":"The ecological and evolutionary significance of frost in the context of climate change","volume":"3","author":"Inouye","year":"2000","journal-title":"Ecol Lett"},{"key":"2025053009565013400_ref38","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1890\/06-2128.1","article-title":"Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers","volume":"89","author":"Inouye","year":"2008","journal-title":"Ecology"},{"key":"2025053009565013400_ref39","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1186\/s13059-020-02154-5","article-title":"GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes","volume":"21","author":"Jin","year":"2020","journal-title":"Genome Biol"},{"key":"2025053009565013400_ref40","doi-asserted-by":"publisher","first-page":"2774","DOI":"10.1002\/ece3.2051","article-title":"Phylosignal: an R package to measure, test, and explore the phylogenetic signal","volume":"6","author":"Keck","year":"2016","journal-title":"Ecol Evol"},{"key":"2025053009565013400_ref41","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1111\/jbi.12238","article-title":"Spring frost and growing season length co-control the cold range limits of broad-leaved trees","volume":"41","author":"Kollas","year":"2014","journal-title":"J Biogeogr"},{"key":"2025053009565013400_ref42","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/j.agrformet.2013.10.001","article-title":"How accurately can minimum temperatures at the cold limits of tree species be extrapolated from weather station data?","volume":"184","author":"Kollas","year":"2014","journal-title":"Agric For Meteorol"},{"key":"2025053009565013400_ref43","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/s00035-011-0089-1","article-title":"Coldest places on earth with angiosperm plant life","volume":"121","author":"K\u00f6rner","year":"2011","journal-title":"Alp Bot"},{"key":"2025053009565013400_ref44","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-0348-0396-0","volume-title":"Alpine treelines: functional ecology of the global high elevation tree limits","author":"K\u00f6rner","year":"2012"},{"key":"2025053009565013400_ref45","volume-title":"Alpine plant life: functional plant ecology of high mountain ecosystems","author":"K\u00f6rner","year":"2021"},{"key":"2025053009565013400_ref46","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1016\/j.tree.2021.06.011","article-title":"The cold range limit of trees","volume":"36","author":"K\u00f6rner","year":"2021","journal-title":"Trends Ecol Evol"},{"key":"2025053009565013400_ref47","doi-asserted-by":"publisher","first-page":"1461","DOI":"10.1126\/science.1186473","article-title":"Phenology under global warming","volume":"327","author":"K\u00f6rner","year":"2010","journal-title":"Science"},{"key":"2025053009565013400_ref48","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.ppees.2017.04.004","article-title":"The 90 ways to describe plant temperature","volume":"30","author":"K\u00f6rner","year":"2018","journal-title":"Perspect Plant Ecol Evol Syst"},{"key":"2025053009565013400_ref49","doi-asserted-by":"publisher","first-page":"1076","DOI":"10.1111\/1365-2745.12574","article-title":"Where, why and how? Explaining the low-temperature range limits of temperate tree species","volume":"104","author":"K\u00f6rner","year":"2016","journal-title":"J Ecol"},{"key":"2025053009565013400_ref50","doi-asserted-by":"publisher","first-page":"1277","DOI":"10.1111\/ele.14260","article-title":"Four ways to define the growing season","volume":"26","author":"K\u00f6rner","year":"2023","journal-title":"Ecol Lett"},{"key":"2025053009565013400_ref51","doi-asserted-by":"publisher","first-page":"436","DOI":"10.1080\/00040851.1991.12002863","article-title":"Effects of snow-free period on the phenology of alpine plants inhabiting snow patches","volume":"23","author":"Kudo","year":"1991","journal-title":"Arct Alp Res"},{"key":"2025053009565013400_ref52","doi-asserted-by":"publisher","first-page":"1300","DOI":"10.2307\/2445714","article-title":"Relationships between flowering time and fruit set of the entomophilous alpine shrub, Rhododendron aureum (Ericaceae), inhabiting snow patches","volume":"80","author":"Kudo","year":"1993","journal-title":"Am J Bot"},{"key":"2025053009565013400_ref53","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/s10144-005-0242-z","article-title":"Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts","volume":"48","author":"Kudo","year":"2006","journal-title":"Popul Ecol"},{"key":"2025053009565013400_ref54","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1007\/s00442-012-2581-8","article-title":"How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment","volume":"171","author":"Ladinig","year":"2013","journal-title":"Oecologia"},{"key":"2025053009565013400_ref55","first-page":"267","article-title":"K\u00e4ltetoleranz und \u00dcberwinterungsverm\u00f6gen mediterraner Holzpflanzen","volume":"5","author":"Larcher","year":"1970","journal-title":"Oecol Plant"},{"key":"2025053009565013400_ref56","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-662-05214-3","volume-title":"Physiological plant ecology","author":"Larcher","year":"2003"},{"key":"2025053009565013400_ref57","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1080\/11263500012331350455","article-title":"Temperature stress and survival ability of Mediterranean sclerophyllous plants","volume":"134","author":"Larcher","year":"2006","journal-title":"Plant Biosyst"},{"key":"2025053009565013400_ref58","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.flora.2008.12.005","article-title":"Survival types of high mountain plants under extreme temperatures","volume":"205","author":"Larcher","year":"2010","journal-title":"Flora"},{"key":"2025053009565013400_ref59","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.1111\/nph.12452","article-title":"European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients","volume":"200","author":"Lenz","year":"2013","journal-title":"New Phytol"},{"key":"2025053009565013400_ref60","doi-asserted-by":"publisher","first-page":"1480","DOI":"10.1111\/1365-2435.12623","article-title":"Convergence of leaf-out towards minimum risk of freezing damage in temperate trees","volume":"30","author":"Lenz","year":"2016","journal-title":"Funct Ecol"},{"key":"2025053009565013400_ref61","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1093\/treephys\/tpv147","article-title":"Fast acclimation of freezing resistance suggests no influence of winter minimum temperature on the range limit of European beech","volume":"36","author":"Lenz","year":"2016","journal-title":"Tree Physiol"},{"key":"2025053009565013400_ref62","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1007\/s10584-007-9327-3","article-title":"Twentieth-century trends in the thermal growing season in the greater Baltic area","volume":"87","author":"Linderholm","year":"2007","journal-title":"Clim Change"},{"key":"2025053009565013400_ref63","doi-asserted-by":"publisher","first-page":"1179","DOI":"10.1111\/jbi.12707","article-title":"Uncovering the spatio-temporal drivers of species trait variances: a case study of Magnoliaceae in China","volume":"43","author":"Liu","year":"2016","journal-title":"J Biogeogr"},{"key":"2025053009565013400_ref64","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1007\/s00035-023-00294-5","article-title":"Phylogeny and phenotypic adjustments drive functional traits in Rhododendron across elevations in its diversity hot-spot in W-China","volume":"133","author":"Liu","year":"2023","journal-title":"Alp Bot"},{"key":"2025053009565013400_ref65","doi-asserted-by":"publisher","first-page":"e0155749","DOI":"10.1371\/journal.pone.0155749","article-title":"Trait-based community assembly along an elevational gradient in subalpine forests: quantifying the roles of environmental factors in inter- and intraspecific variability","volume":"11","author":"Luo","year":"2016","journal-title":"PloS One"},{"key":"2025053009565013400_ref66","doi-asserted-by":"publisher","first-page":"3818","DOI":"10.1111\/1365-2745.13759","article-title":"Functional traits shape tree species distribution in the Himalayas","volume":"109","author":"Maharjan","year":"2021","journal-title":"J Ecol"},{"key":"2025053009565013400_ref67","first-page":"1","volume-title":"In proceedings of the gateway computing environments workshop (GCE)","author":"Miller","year":"2010"},{"key":"2025053009565013400_ref68","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1007\/s00035-020-00236-5","article-title":"Does the life-history strategy determine the freezing resistance of flowers and leaves of alpine herbaceous species?","volume":"130","author":"Morales","year":"2020","journal-title":"Alp Bot"},{"key":"2025053009565013400_ref69","doi-asserted-by":"publisher","first-page":"105332","DOI":"10.1016\/j.envexpbot.2023.105332","article-title":"When sunlight goes out, avoidance mechanisms are defective for protecting flowers from freezing damage","volume":"210","author":"Morales","year":"2023","journal-title":"Environ Exp Bot"},{"key":"2025053009565013400_ref70","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1111\/j.1461-0248.2011.01601.x","article-title":"Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured","volume":"14","author":"Mungu\u00eda-Rosas","year":"2011","journal-title":"Ecol Lett"},{"key":"2025053009565013400_ref71","first-page":"50","article-title":"Assessment of foliar frost damage: a comparison of chlorophyll fluorescence with other viability tests","volume":"73","author":"Neuner","year":"1999","journal-title":"J Appl Bot Food Qual"},{"key":"2025053009565013400_ref72","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/978-3-7091-0136-0_12","volume-title":"Plants in alpine regions: Cell physiology of adaption and survival strategies","author":"Neuner","year":"2012"},{"key":"2025053009565013400_ref73","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1016\/s0367-2530(17)30916-7","article-title":"Readiness to frost harden during the dehardening period measured in situ in leaves of Rhododendron ferrugineum L. at the alpine timberline","volume":"194","author":"Neuner","year":"1999","journal-title":"Flora"},{"key":"2025053009565013400_ref74","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1111\/j.1399-3054.2012.01616.x","article-title":"Frost resistance of reproductive tissues during various stages of development in high mountain plants","volume":"147","author":"Neuner","year":"2013","journal-title":"Physiol Plant"},{"key":"2025053009565013400_ref75","doi-asserted-by":"publisher","DOI":"10.1016\/j.envexpbot.2019.103882","article-title":"Low temperatures at higher elevations require plants to exhibit increased freezing resistance throughout the summer months","volume":"169","author":"Neuner","year":"2020","journal-title":"Environ Exp Bot"},{"key":"2025053009565013400_ref76","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1038\/44766","article-title":"Inferring the historical patterns of biological evolution","volume":"401","author":"Pagel","year":"1999","journal-title":"Nature"},{"key":"2025053009565013400_ref77","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1007\/s11258-005-9081-4","article-title":"Carbon sink limitation and frost tolerance control performance of the tree Kageneckia angustifolia D. Don (Rosaceae) at the treeline in Central Chile","volume":"185","author":"Piper","year":"2005","journal-title":"Plant Ecol"},{"key":"2025053009565013400_ref78","first-page":"54","article-title":"Versuche zur Frostresistenzpr\u00fcfung von Rinde, Winterknospen und Bl\u00fcten einiger Arten von Obsth\u00f6lzern","volume":"23","author":"Pisek","year":"1958","journal-title":"Gartenbauwissenschaft"},{"key":"2025053009565013400_ref79","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1146\/annurev.es.18.110187.002205","article-title":"Relationships among flowers, fruits, and seeds","volume":"18","author":"Primack","year":"1987","journal-title":"Annu Rev Ecol Syst"},{"key":"2025053009565013400_ref80","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1186\/s13007-019-0435-7","article-title":"PGA: a software package for rapid, accurate, and flexible batch annotation of plastomes","volume":"15","author":"Qu","year":"2019","journal-title":"Plant Methods"},{"key":"2025053009565013400_ref81","doi-asserted-by":"publisher","first-page":"e16505","DOI":"10.7717\/peerj.16505","article-title":"Phytools 2.0: an updated R ecosystem for phylogenetic comparative methods (and other things)","volume":"12","author":"Revell","year":"2024","journal-title":"PeerJ"},{"key":"2025053009565013400_ref82","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/S0304-4238(99)00150-8","article-title":"Spring frosts in deciduous fruit trees. Morphological damage and flower hardiness","volume":"85","author":"Rodrigo","year":"2000","journal-title":"Sci Hortic"},{"key":"2025053009565013400_ref83","doi-asserted-by":"publisher","first-page":"485","DOI":"10.2307\/1935383","article-title":"Freezing resistance in willows from different climates","volume":"51","author":"Sakai","year":"1970","journal-title":"Ecology"},{"key":"2025053009565013400_ref84","first-page":"91","article-title":"Freezing resistance of conifers","volume":"20","author":"Sakai","year":"1971","journal-title":"Silvae Genet"},{"key":"2025053009565013400_ref85","doi-asserted-by":"publisher","first-page":"2323","DOI":"10.1139\/b83-255","article-title":"Comparative study on freezing resistance of conifers with special reference to cold adaptation and its evolutive aspects","volume":"61","author":"Sakai","year":"2011","journal-title":"Can J Bot"},{"key":"2025053009565013400_ref86","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-71745-1","volume-title":"Frost survival of plants: Responses and adaptations to freezing stress","author":"Sakai","year":"1987"},{"key":"2025053009565013400_ref87","doi-asserted-by":"publisher","first-page":"563","DOI":"10.2307\/1937722","article-title":"Freezing resistance of trees of the south temperate zone, especially subalpine species of Australasia","volume":"62","author":"Sakai","year":"1981","journal-title":"Ecology"},{"key":"2025053009565013400_ref88","doi-asserted-by":"crossref","first-page":"273","DOI":"10.21273\/JASHS.111.2.273","article-title":"Cold hardniess in the genus Rhododendron","volume":"111","author":"Sakai","year":"1986","journal-title":"J Am Soc Hort Sci"},{"key":"2025053009565013400_ref89","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1002\/ajb2.1222","article-title":"A temporal shift in resource allocation facilitates flowering before leaf out and spring vessel maturation in precocious species","volume":"106","author":"Savage","year":"2019","journal-title":"Am J Bot"},{"key":"2025053009565013400_ref90","first-page":"33","article-title":"Die Temperaturbeeinflu\u00dfbarkeit der Frosth\u00e4rte von Nadelh\u00f6lzern und Zwergstr\u00e4uchern an der alpinen Waldgrenze","volume":"47","author":"Schie\u00dfl","year":"1947","journal-title":"Ber Naturwiss Med Ver Innsbruck"},{"key":"2025053009565013400_ref91","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1111\/nph.13234","article-title":"As old as the mountains: the radiations of the Ericaceae","volume":"207","author":"Schwery","year":"2015","journal-title":"New Phytol"},{"key":"2025053009565013400_ref92","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1111\/geb.12750","article-title":"Global patterns of Rhododendron diversity: the role of evolutionary time and diversification rates","volume":"27","author":"Shrestha","year":"2018","journal-title":"Glob Ecol Biogeogr"},{"key":"2025053009565013400_ref93","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1080\/02827589509382862","article-title":"No difference in frost hardiness between high and low altitude Pinus sylvestris (L.) offspring","volume":"10","author":"Sundblad","year":"2008","journal-title":"Scand J For Res"},{"key":"2025053009565013400_ref94","doi-asserted-by":"publisher","first-page":"110520","DOI":"10.1016\/j.scienta.2021.110520","article-title":"A 15-year long assessment of cold hardiness of apricot flower buds and flowers during the blooming period","volume":"290","author":"Szalay","year":"2021","journal-title":"Sci Hortic"},{"key":"2025053009565013400_ref95","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1111\/j.1365-3040.2004.01176.x","article-title":"Summer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary","volume":"27","author":"Taschler","year":"2004","journal-title":"Plant Cell Environ"},{"key":"2025053009565013400_ref96","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1093\/treephys\/24.3.331","article-title":"Frost resistance and ice nucleation in leaves of five woody timberline species measured in situ during shoot expansion","volume":"24","author":"Taschler","year":"2004","journal-title":"Tree Physiol"},{"key":"2025053009565013400_ref97","doi-asserted-by":"publisher","first-page":"W232","DOI":"10.1093\/nar\/gkw256","article-title":"W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis","volume":"44","author":"Trifinopoulos","year":"2016","journal-title":"Nucleic Acids Res"},{"key":"2025053009565013400_ref98","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1111\/1365-2745.12251","article-title":"Earlier leaf-out rather than difference in freezing resistance puts juvenile trees at greater risk of damage than adult trees","volume":"102","author":"Vitasse","year":"2014","journal-title":"J Ecol"},{"key":"2025053009565013400_ref99","doi-asserted-by":"publisher","first-page":"541","DOI":"10.3389\/fpls.2014.00541","article-title":"The interaction between freezing tolerance and phenology in temperate deciduous trees","volume":"5","author":"Vitasse","year":"2014","journal-title":"Front Plant Sci"},{"key":"2025053009565013400_ref100","doi-asserted-by":"publisher","first-page":"1562","DOI":"10.1111\/jbi.14455","article-title":"Low winter temperatures and divergent freezing resistance set the cold range limit of widespread alpine graminoids","volume":"49","author":"Von B\u00fcren","year":"2022","journal-title":"J Biogeogr"},{"key":"2025053009565013400_ref101","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1007\/s00035-020-00245-4","article-title":"Elevation-specific responses of phenology in evergreen oaks from their low-dry to their extreme high-cold range limits in the SE Himalaya","volume":"131","author":"Wang","year":"2021","journal-title":"Alp Bot."},{"key":"2025053009565013400_ref102","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1657\/1523-0430(06-066)[wardle]2.0.Co;2","article-title":"New Zealand Forest to alpine transitions in global context","volume":"40","author":"Wardle","year":"2008","journal-title":"Arct Antarct Alp Res"},{"key":"2025053009565013400_ref103","doi-asserted-by":"publisher","first-page":"msab314","DOI":"10.1093\/molbev\/msab314","article-title":"Spatiotemporal evolution of the global species diversity of Rhododendron","volume":"39","author":"Xia","year":"2022","journal-title":"Mol Biol Evol"},{"key":"2025053009565013400_ref104","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1093\/treephys\/tpaa070","article-title":"Explaining the exceptional 4270 m high elevation limit of an evergreen oak in the south-eastern Himalayas","volume":"40","author":"Yang","year":"2020","journal-title":"Tree Physiol"},{"key":"2025053009565013400_ref105","doi-asserted-by":"publisher","first-page":"1244","DOI":"10.1111\/jse.12690","article-title":"Joint effect of phylogenetic relatedness and trait selection on the elevational distribution of Rhododendron species","volume":"59","author":"Zou","year":"2021","journal-title":"J Syst Evol"}],"container-title":["Tree Physiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/treephys\/advance-article-pdf\/doi\/10.1093\/treephys\/tpaf036\/62749777\/tpaf036.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/treephys\/article-pdf\/45\/5\/tpaf036\/62749777\/tpaf036.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/treephys\/article-pdf\/45\/5\/tpaf036\/62749777\/tpaf036.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,5,30]],"date-time":"2025-05-30T09:57:10Z","timestamp":1748599030000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/treephys\/article\/doi\/10.1093\/treephys\/tpaf036\/8096612"}},"subtitle":[],"editor":[{"given":"Benedicte","family":"Wenden","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,3,26]]},"references-count":105,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2025,5,2]]}},"URL":"https:\/\/doi.org\/10.1093\/treephys\/tpaf036","relation":{},"ISSN":["1758-4469"],"issn-type":[{"value":"1758-4469","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,5]]},"published":{"date-parts":[[2025,3,26]]},"article-number":"tpaf036"}}