In 1998, Bill Gray and colleagues showed that warm temperatures trigger arabidopsis hypocotyl elongation in an auxin-dependent manner. This laid the foundation for a vibrant research discipline. With several active members of the 'thermomorphogenesis' community, we here reflect on 25 years of elevated ambient temperature research and look to the future

Balasubramanian, Sureshkumar

Balcerowicz, Martin

Casal, Jorge J

Castroverde, Christian Danve M

Chen, Meng

Chen, Xuemei

De Smet, Ive

Delker, Carolin

Fankhauser, Christian

Franklin, Keara A

Halliday, Karen J

Hayes, Scott

Jiang, Danhua

Jung, Jae-Hoon

Kaiserli, Eirini

Kumar, S Vinod

Maag, Daniel

Oh, Eunkyoo

Park, Chung-Mo

Penfield, Steven

Perrella, Giorgio

Prat, Salomé

Quint, Marcel

Reis, Rodrigo S

van Zanten, Martijn

Wigge, Philip A

Willige, Björn C

Utrecht University Repository

Trends inPlant ScienceForum25 Years ofthermomorphogenesisresearch: milestonesand perspectivesMarcel Quint ,1,31,33,*1Carolin Delker ,SureshkumarBalasubramanian ,2,@Martin Balcerowicz ,3,@Jorge J. Casal ,4,5Christian Danve M.Castroverde ,6,@Meng Chen ,7,@Xuemei Chen ,8,@Ive De Smet ,9,10,@Christian Fankhauser ,11,@Keara A. Franklin ,12Karen J. Halliday,13Scott Hayes ,14,@Danhua Jiang ,15Jae-Hoon Jung ,16,@Eirini Kaiserli ,17S. Vinod Kumar ,18Daniel Maag ,19Eunkyoo Oh ,20Chung-Mo Park ,21,22Steven Penfield ,23Giorgio Perrella ,24,@Salomé Prat ,25Rodrigo S. Reis ,26,@Philip A. Wigge ,27,28,@Björn C. Willige ,29,@ andMartijn van Zanten 30,32,33,*,@In 1998, Bill Gray and colleaguesshowed that warm temperaturestrigger arabidopsis hypocotylelongation in an auxin-dependentmanner. This laid the foundationfor a vibrant research discipline.With several active members ofthe ‘thermomorphogenesis’ com-munity, we here reflect on 25 years1098 Trends in Plant Science, October 2023, Vol. 28, No. 1of elevated ambient temperatureresearch and look to the future.The beginningIn the early days of molecular genetics,temperature-sensitive mutants becamea tool for the dissection of molecularpathways. In the late 1970s, for example,essential genes regulating the buddingyeast secretory pathway were identifiedin this manner [1]. Being trained as ayeast geneticist, Bill (William) Gray, a post-doc in Mark Estelle’s laboratory at IndianaUniversity (USA), and colleagues used asimilar approach in Arabidopsis thaliana(hereafter arabidopsis). Bill aimed toidentify temperature-sensitive alleles ofTRANSPORT INHIBITOR RESPONSE 1(TIR1), which was at the time an unknownauxin coreceptor. Although he was notsuccessful in identifying such tir1 alleles,his observation that elevated temperaturepromotes auxin-mediated hypocotyl elon-gation [2] would lay the foundation for athriving research discipline known nowas thermomorphogenesis. This year theengaged and active thermomorphogenesiscommunity celebrates its 25th anniversary(Figure 1).The Gray study provided the basis for amolecular framework to understand thephysiological responses to elevated ambienttemperatures. Subsequently, work from theFranklin laboratory provided importantinsights into the potential benefits that plantsobtain from thermomorphogenic growthpatterns by showing that, in particular,petiole elongation and hyponastic growthare associated with increased transpirationand lower leaf temperatures (Figure 1A).This indicates that thermomorphogenesisstimulates leaf cooling by enhancing evapo-ration, suggesting a possible functional rele-vance to plants, at least under laboratoryconditions [3]. However, in natural and agri-cultural settings the situation is undoubtedlymore complex as plants have to deal with0multiple environmental factors at the sametime (see also later).Molecular signalling andthermosensingThe publication of Gray’s seminal results [2]did not immediately spark follow-up studies.It was not until 2009, when the Franklinlaboratory identified the bHLH transcriptionfactor PHYTOCHROME-INTERACTINGFACTOR 4 (PIF4) [4] as a key regulatorof thermomorphogenic signalling, pavingthe way for subsequent discoveriesincluding the identification of the firstthermosensors. In the same year, a secondimportant study was published, describinggibberellins and brassinosteroids as phyto-hormones that, in addition to auxin, coordi-nate thermosensitive shoot growth [5],as we now know, downstream of PIF4.These two papers [4,5], together with thefinding that PIF4 directly regulates specificauxin biosynthesis genes like YUCCA8[6,7], inspired many scientists. Increasingnumbers of groups from related disciplines(photobiology, phytohormone biology,natural variation, flowering regulation,epigenetics, thermotolerance, cellularsignalling, immunity, post-transcriptionalregulation, miRNA biogenesis) steppedin and started to elucidate how plantsrespond to elevated ambient tempera-tures. Not least, the research interestwas fuelled by the emerging awarenessof rapid global warming and the needto harness crops to safeguard foodsecurity. The prospect of contributing toclimate change mitigation is still a majordriver for many of the authors of this forumto devote resources to gain fundamentalknowledge on thermomorphogenesis regu-lation and understanding of its functionalconsequences.Studying warm temperature signalling isnot a trivial task because temperature,being essentially molecular motion, is aversatile signal and has no ligand proper-ties nor distinct physical features. Formany years, it therefore remained unclear1850sH2A.ZHSP70YUC8PIF4IAAG-boxPIF4GA BRELF3PIF75'-PIF75'-IAA1998 200920102011 2012IAA2019phyBPr Pfr20162020(B)Reproductive phenologyHyponastystem elongationRoot elongationLeaf expansion Petiole elongation(A)Trends in Plant ScienceFigure 1. Milestones in 25 years of thermomorphogenesis research. (A) Model thermomorphogenicphenotypes represented on a stylised plant; arrows indicate thermo-induced directions of the correspondingphenotypes. (B) Roadmap of selected important research milestones, starting with the discovery that the auxinindole-3-acetic acid (IAA) mediates temperature-dependent hypocotyl elongation and leading towards thegeneration of future climate-resilient crops; colours of the centreline markings indicate the global temperaturechange relative to the 1971–2000 average, based on information from https://showyourstripes.info/c/globe witheach stripe representing 1 year. Blue and red colours indicate below-average and above-average temperatures,respectively, with darker colours indicating greater deviations from the mean. Abbreviations: ELF3, EARLYFLOWERING 3; PIF4, PHYTOCHROME-INTERACTING FACTOR 4; phyB, phytochrome B.Trends in Plant Sciencewhether specific thermosensors hadevolved in plants. Finding bona fidethermosensors has been, and remains, amajor goal. Although not entailing a dedi-cated sensor, a warm temperature relaycascade was uncovered by the Wiggelaboratory in 2010, showing that evictionof the noncanonical histone H2A.Z fromthe chromatin of temperature-induciblegenes is required for thermomorphogenicresponses [8]. Building on earlier workfrom the Whitelam, Schäfer, and Hallidaylaboratories, the Wigge and Casal labo-ratories showed that phytochrome B(phyB) is a thermosensor using a combi-nation of omics, biochemistry, spectros-copy, and genetics, hence revealingthat thermomorphogenesis requires asurveillance system directly linked tolight responses [9,10]. Subsequently,temperature-dependent phase transitionof EARLY FLOWERING 3 (ELF3) into bio-molecular condensates and temperature-dependent conformational changes inthe PIF7 mRNA structure resulting inenhanced translation were shown toalso sense temperature changes [11,12].Thus, various thermosensing mechanismsat the DNA, RNA, and protein levels havebeen uncovered and more are expectedto be found.Where do we go from here?Based on the early findings on the in-volvement of PIF4, auxin, and other hor-mones [2,4–7], and by the identificationof thermosensory mechanisms, thermo-morphogenesis has become an establishedTrefield in the plant sciences. However, manyimportant points remain to be addressed.One major question is the spatial andtemporal regulation of thermomorphogenicresponses across organs and tissues,down to potential cell-type specificities.Although a number of studies have spe-cifically addressed this issue (e.g., [13]),we are only now beginning to understandthe communication of temperature sig-nals within the plant. Another challengeis to distinguish whether specific thermo-morphogenic signalling events exist andto distinguish these from thermodynamiceffects on several (if not all) signalling net-works, given that temperature impactsevery molecule and reaction in the plant,including enzyme activities. This alsoraises the question of how cold, ambientwarm, and heat (tolerance) responsesare, if at all, connected. A gradient ap-proach may reveal for example, whethercold regulators are involved in warm tem-perature responses and vice versa andthus whether there exists a generic re-sponse to temperature or whether distinctsignalling branches deal with differenttemperature cues. Part of the answermay be obtained by taking an epigeneticapproach, as regulation of different levelsof histone H3 lysine 4 methylation appearsto be a signalling hub where diverse tem-perature cues converge [14].At the organismal level, a potential pitfallof thermomorphogenesis research is thatfunctional hypotheses are relatively easyto formulate when only temperature is con-sidered. For example, temperature-inducedroot elongation may serve to reach deeperwater to meet the demands of increasedtranspiration and hyponasty is likely toreduce heat flux on the leaves. However,the contribution of thermomorphogenesisand its component traits in natural environ-ments is complex and currently not wellunderstood. One avenue of future researchshould focus on understanding whichthermomorphogenic responses contributeto plant performance in the wild and/ornds in Plant Science, October 2023, Vol. 28, No. 10 1099Trends in Plant Scienceagricultural environments, what fitnesscosts are associated, and which regula-tors of the canonical or peripheral path-ways are targeted by natural selectionto confer a selective advantage. Whilethe community has so far gained under-standing of thermomorphogenesis underhighly controlled conditions, it is time toexpand beyond the laboratory to studythermomorphogenesis in wild speciesand in crops. It has been reported thatthermomorphogenesis does occur inseveral crop species such as cabbage,tomato, and wheat [15], but the mo-lecular mechanisms need to be furtherexplored to be able to contribute tothe generation of climate-resilient vari-eties (Figure 1B). Emphasis should beplaced on the interaction with bioticsignals and their potential trade-offs.Global warming will increase pathogenpressure, highlighting the importance ofbetter understanding the interactions be-tween temperature and the biotic environ-ment, which may also apply vice versa tomicroorganisms that positively influenceplant performance in symbiotic interac-tions. In addition, temperature will influencethe way in which abiotic factors such asdrought or salt stress are perceived anddealt with. For example, while warm tem-perature episodes often co-occur withdrought, there is an apparent conflict intheir optimal responses, since drought-induced stomatal closure may preventleaf cooling facilitated through increasedthermomorphogenesis-mediated transpi-ration. The crosstalk and potential primingrole of thermomorphogenesis in thermotol-erance (e.g., do thermomorphogenesissignalling and resulting phenotypes con-tribute to heat stress survival?) is an-other critical point that requires furtherinvestigation.Perhaps the greatest challenge for thermo-morphogenesis research lies in translation:how do we exploit conceptual break-throughs in understanding temperaturesignalling to engineer plant resilience in1100 Trends in Plant Science, October 2023, Vol. 28, No. 1this era of unprecedented global warming?Despite excellent progress on understand-ing the mechanisms underlying individualthermomorphogenic responses over thepast 25 years, we may have bigger discov-eries to come.AcknowledgmentsMany laboratories have made important contributionsto the field. We sincerely apologise to all those whoseimportant work could not be included due to stringentspace and referencing constraints.Declaration of interestsNo interests are declared.1Institute of Agricultural and Nutritional Sciences, Martin LutherUniversity Halle-Wittenberg, 06120 Halle (Saale), Germany2School of Biological Sciences, Monash University,Clayton Campus, VIC 3800, Australia3Division of Plant Sciences, University of Dundee at the JamesHutton Institute, Dundee DD2 5DA, UK4IFEVA, Universidad de Buenos Aires and CONICET,1417 Buenos Aires, Argentina5Fundación Instituto Leloir, C1405 BWE, Buenos Aires,Argentina6Department of Biology, Wilfrid Laurier University, Waterloo,Ontario N2L 3C5, Canada7Department of Botany and Plant Sciences, University ofCalifornia, Riverside, Riverside, CA 92521, USA8School of Life Sciences, Peking University, Beijing 100871,China9Department of Plant Biotechnology and Bioinformatics,Ghent University, B-9052 Ghent, Belgium10VIB Center for Plant Systems Biology, B-9052 Ghent, Belgium11Center for Integrative Genomics, Faculty of Biology and Medicine,University of Lausanne, CH-1015 Lausanne, Switzerland12University of Bristol, Bristol BS8 1TQ, UK13Institute of Molecular Plant Sciences, School of BiologicalSciences, University of Edinburgh, Edinburgh 3H9 3BF, UK14Laboratory of Plant Physiology, Wageningen University &Research, 6708 PB Wageningen, The Netherlands15Institute of Genetics and Developmental Biology,Chinese Academy of Sciences, 100101 Beijing, China16Department of Biological Sciences, SungkyunkwanUniversity, 16419 Suwon, South Korea17School of Molecular Biosciences, College of Medical,Veterinary and Life Sciences, University of Glasgow,Glasgow G12 8QQ, UK18Department of Biosciences, University of Exeter, Exeter EX44QD, UK19Department of Pharmaceutical Biology, Julius von SachsInstitute of Biosciences, University of Würzburg, 97082Würzburg, Germany20Department of Life Sciences, Korea University, 02841 Seoul,Korea21Department of Chemistry, Seoul National University, 08826Seoul, Korea22Plant Genomics and Breeding Institute, Seoul NationalUniversity, 08826 Seoul, Korea23Department of Crop Genetics, John Innes Centre, NorwichNR4 7UH, UK24Department of Biosciences, University of Milan, 20133 Milan,Italy25Department of Plant Responses to Stress, Centre forResearch in Agricultural Genomics (CRAG), Campus UAB,08193 Cerdanyola, Barcelona, Spain026Institute of Plant Sciences, University of Bern, 3013 Bern,Switzerland27Leibniz Institut für Gemüse und Zierpflanzenbau, 14979Großbeeren, Germany28Institute of Biochemistry and Biology, University of Potsdam,14476 Potsdam, Germany29Department of Soil and Crop Sciences, Colorado StateUniversity, Fort Collins, CO 80521, USA30Plant Stress Resilience, Institute of Environmental Biology,Utrecht University, 3584 CH Utrecht, The Netherlands31https://quintlab.landw.uni-halle.de32https://www.uu.nl/en/research/plant-stress-resilience33Equal contributions*Correspondence:marcel.quint@landw.uni-halle.de (M. Quint) andm.vanzanten@uu.nl (M. van Zanten).@Twitter: @skblab (S. Balasubramanian), @tran_scription(M. Balcerowicz), @DanveC (C.D.M. Castroverde),@MengChen_Lab (M. Chen), @Xuemei_RNAlab (X. Chen),@IveDeSmet1978 (I. De Smet), @FankhauserCh(C. Fankhauser), @scotanist (S. Hayes), @JungLab_SKKU(J-H. Jung), @GioPerrella26 (G. Perrella), @Rodrigo_S_Reis(R.S. Reis), @PhilWigge (P.A. Wigge), @BjornWillige(B.C. Willige), and @zantenMartijn and @UU-Plants(M. van Zanten).https://doi.org/10.1016/j.tplants.2023.07.001© 2023 Elsevier Ltd. All rights reserved.References1. Novick, P. et al. (1980) Identification of 23 complementa-tion groups required for post-translational events in theyeast secretory pathway. Cell 21, 205–2152. Gray, W.M. et al. (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl.Acad. Sci. U. S. A. 95, 7197–72023. Crawford, A.J. et al. (2012) High temperature exposure in-creases plant cooling capacity. Curr. Biol. 22, R396–R3974. Koini, M. et al. (2009) High temperature-mediated adapta-tions in plant architecture require the bHLH transcriptionfactor PIF4. Curr. Biol. 19, 408–4135. Stavang, J.A. et al. (2009) Hormonal regulation oftemperature-induced growth in Arabidopsis. Plant J. 60,589–6016. Franklin, K.A. et al. (2011) Phytochrome-interacting factor4 (PIF4) regulates auxin biosynthesis at high temperature.Proc. Natl. Acad. Sci. U. S. A. 108, 20231–202357. Sun, J. et al. (2012) PIF4-mediated activation of YUCCA8expression integrates temperature into the auxin pathwayin regulating arabidopsis hypocotyl growth. PLoS Genet.8, e10025948. Kumar, S.V. and Wigge, P.A. (2010) H2A.Z-containingnucleosomes mediate the thermosensory response inArabidopsis. Cell 140, 136–1479. Jung, J.-H. et al. (2016) Phytochromes function asthermosensors in Arabidopsis. Science 354, 886–88910. Legris, M. et al. (2016) Phytochrome B integrates light andtemperature signals in Arabidopsis. Science 354, 897–90011. Chung, B.Y.W. et al. (2020) An RNA thermoswitch regulatesdaytime growth in Arabidopsis. Nat. Plants 6, 522–53212. Jung, J.-H. et al. (2020) A prion-like domain in ELF3 functionsas a thermosensor in Arabidopsis. Nature 585, 256–26013. Bellstaedt, J. et al. (2019) A mobile auxin signal connectstemperature sensing in cotyledons with growth responsesin hypocotyls. Plant Physiol. 180, 757–76614. Perrella, G. et al. (2022) Epigenetic regulation of thermo-morphogenesis and heat stress tolerance. New Phytol.234, 1144–116015. Zhu, T. et al. (2021) The heat is on: how crop growth,development and yield respond to high temperature.J. Exp. Bot. 72, 7359–7373

25 Years of thermomorphogenesis research: milestones and perspectives

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25 Years of thermomorphogenesis research: milestones and perspectives

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