The size of plant organs is highly responsive to environmental conditions. The plant's embryonic stem, or hypocotyl, displays phenotypic plasticity, in response to light and temperature. The hypocotyl of shade avoiding species elongates to outcompete neighboring plants and secure access to sunlight. Similar elongation occurs in high temperature. However, it is poorly understood how environmental light and temperature cues interact to effect plant growth. We found that shade combined with warm temperature produces a synergistic hypocotyl growth response that dependent on PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) and auxin. This unique but agriculturally relevant scenario was almost totally independent on PIF4 activity. We show that warm temperature is sufficient to promote PIF7 DNA binding but not transcriptional activation and we demonstrate that additional, unknown factor/s must be working downstream of the phyB-PIF-auxin module. Our findings will improve the predictions of how plants will respond to increased ambient temperatures when grown at high density.

Howard Hughes Medical Institute Salk Institute for Biological Studies La Jolla CA 92037 USA

Institute of Plant Sciences ARO Volcani Institute HaMaccabbim Road 68 Rishon LeZion 7505101 Israel

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Šlechtitelů 27 CZ 78371 Olomouc Czech Republic

Plant Biology Laboratory Salk Institute for Biological Studies 10010 North Torrey Pines Road La Jolla CA 92037 USA

Umeå Plant Science Centre Department of Forest Genetics and Plant Physiology Swedish University of Agricultural Sciences SE 901 83 Umeå Sweden

Zobrazit více v PubMed

Casal JJ. Shade avoidance. Arabidopsis Book. 2012;10:e0157. doi: 10.1199/tab.0157. PubMed DOI PMC

Ballare CL, Sanchez RA, Scopel AL, Casal JJ, Ghersa CM. Early detection of neighbour plants by phytochrome perception of spectral changes in reflected sunlight. Plant, Cell Environ. 1987;10:551–557.

Ballare CL, Scopel AL, Sanchez RA. Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science. 1990;247:329–332. doi: 10.1126/science.247.4940.329. PubMed DOI

Smith H, Whitelam GC. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant, Cell Environ. 1997;20:840–844. doi: 10.1046/j.1365-3040.1997.d01-104.x. DOI

Casal JJ, Balasubramanian S. Thermomorphogenesis. Annu. Rev. Plant Biol. 2019;70:321–346. doi: 10.1146/annurev-arplant-050718-095919. PubMed DOI

Wall JK, Johnson CB. The effect of temperature on phytochrome controlled hypocotyl extension in Sinapis alba L. N. Phytologist. 1982;91:405–412. doi: 10.1111/j.1469-8137.1982.tb03319.x. DOI

Weinig C. Limits to adaptive plasticity: Temperature and photoperiod influence shade-avoidance responses. Am. J. Bot. 2000;87:1660–1668. doi: 10.2307/2656743. PubMed DOI

Halliday KJ, Salter MG, Thingnaes E, Whitelam GC. Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J. 2003;33:875–885. doi: 10.1046/j.1365-313X.2003.01674.x. PubMed DOI

Patel D, et al. Temperature-dependent shade avoidance involves the receptor-like kinase ERECTA. Plant J. 2013;73:980–992. doi: 10.1111/tpj.12088. PubMed DOI

Romero‐Montepaone S, et al. Shade avoidance responses become more aggressive in warm environments. Plant, Cell Environ. 2020;43:1625–1636. doi: 10.1111/pce.13720. PubMed DOI

Jung J-H, et al. Phytochromes function as thermosensors in Arabidopsis. Science. 2016;354:886–889. doi: 10.1126/science.aaf6005. PubMed DOI

Legris, M. et al. Phytochrome B integrates light and temperature signals in Arabidopsis. Science354, 897–900 (2016). PubMed

Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell. 1993;5:147–157. PubMed PMC

Smth H, Holmes MG. The function of phytochrome in the natural environment—III. Measurement and calculation of phytochrome photoequilibria. Photochemistry Photobiol. 1977;25:547–550. doi: 10.1111/j.1751-1097.1977.tb09126.x. DOI

Gangappa SN, Kumar SV. DET1 and HY5 control PIF4-mediated thermosensory elongation growth through distinct mechanisms. Cell Rep. 2017;18:344–351. doi: 10.1016/j.celrep.2016.12.046. PubMed DOI PMC

Qiu Y, Li M, Kim RJA, Moore CM, Chen M. Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA. Nat. Commun. 2019;10:140–140. doi: 10.1038/s41467-018-08059-z. PubMed DOI PMC

Lee, S., Paik, I. & Huq, E. SPAs promote thermomorphogenesis by regulating the phyB-PIF4 module in Arabidopsis. Development147, dev189233 (2020). PubMed PMC

Vu LD, Xu X, Gevaert K, De Smet I. Developmental plasticity at high temperature. Plant Physiol. 2019;181:399–411. doi: 10.1104/pp.19.00652. PubMed DOI PMC

Fiorucci A-S, et al. PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to elevated temperature in Arabidopsis seedlings. N. Phytologist. 2020;226:50–58. doi: 10.1111/nph.16316. PubMed DOI PMC

Chung BYW, et al. An RNA thermoswitch regulates daytime growth in Arabidopsis. Nat. Plants. 2020;6:522–532. doi: 10.1038/s41477-020-0633-3. PubMed DOI PMC

Galvāo VC, et al. PIF transcription factors link a neighbor threat cue to accelerated reproduction in Arabidopsis. Nat. Commun. 2019;10:4005–4005. doi: 10.1038/s41467-019-11882-7. PubMed DOI PMC

Huang X, et al. Shade-induced nuclear localization of PIF7 is regulated by phosphorylation and 14-3-3 proteins in Arabidopsis. eLife. 2018;7:470–476. PubMed PMC

Willige BC, et al. Phytochrome-interacting factors trigger environmentally responsive chromatin dynamics in plants. Nat. Genet. 2021;53:955–961. doi: 10.1038/s41588-021-00882-3. PubMed DOI PMC

de Wit M, Ljung K, Fankhauser C. Contrasting growth responses in lamina and petiole during neighbor detection depend on differential auxin responsiveness rather than different auxin levels. N. Phytol. 2015;208:198–209. doi: 10.1111/nph.13449. PubMed DOI

Li L, et al. Linking photoreceptor excitation to changes in plant architecture. Genes Dev. 2012;26:785–790. doi: 10.1101/gad.187849.112. PubMed DOI PMC

Kohnen MV, et al. Neighbor detection induces organ-specific transcriptomes, revealing patterns underlying hypocotyl-specific growth. Plant Cell. 2016;28:2889–2904. doi: 10.1105/tpc.16.00463. PubMed DOI PMC

Bellstaedt, J. et al. A mobile auxin signal connects temperature sensing in cotyledons with growth responses in hypocotyls. Plant Physiol.180, 757–766 (2019). PubMed PMC

Procko C, Crenshaw CM, Ljung K, Noel JP, Chory J. Cotyledon-generated auxin is required for shade-induced hypocotyl growth in Brassica rapa. Plant Physiol. 2014;165:1285–1301. doi: 10.1104/pp.114.241844. PubMed DOI PMC

Procko C, et al. The epidermis coordinates auxin-induced stem growth in response to shade. Genes Dev. 2016;30:1529–1541. doi: 10.1101/gad.283234.116. PubMed DOI PMC

Müller-Moulé P, et al. YUCCA auxin biosynthetic genes are required for Arabidopsis shade avoidance. PeerJ. 2016;4:e2574–e2574. doi: 10.7717/peerj.2574. PubMed DOI PMC

Kozuka T, et al. Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol. 2010;153:1608–1618. doi: 10.1104/pp.110.156802. PubMed DOI PMC

Chapman EJ, et al. Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS ONE. 2012;7:e36210. doi: 10.1371/journal.pone.0036210. PubMed DOI PMC

Stavang JA, et al. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 2009;60:589–601. doi: 10.1111/j.1365-313X.2009.03983.x. PubMed DOI

Bours R, Kohlen W, Bouwmeester HJ, van der Krol A. Thermoperiodic control of hypocotyl elongation depends on auxin-induced ethylene signaling that controls downstream Phytochrome interacting factor3 activity. Plant Physiol. 2015;167:517–530. doi: 10.1104/pp.114.254425. PubMed DOI PMC

Franklin KA, et al. Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl Acad. Sci. USA. 2011;108:20231–20235. doi: 10.1073/pnas.1110682108. PubMed DOI PMC

Kumar SV, et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature. 2012;484:242–245. doi: 10.1038/nature10928. PubMed DOI PMC

Vu LD, et al. The membrane-localized protein kinase MAP4K4/TOT3 regulates thermomorphogenesis. Nat. Commun. 2021;12:2842. doi: 10.1038/s41467-021-23112-0. PubMed DOI PMC

Pedmale UV, et al. Cryptochromes interact directly with PIFs to control plant growth in limiting blue light. Cell. 2016;164:233–245. doi: 10.1016/j.cell.2015.12.018. PubMed DOI PMC

Ma D, et al. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc. Natl Acad. Sci. USA. 2016;113:224–229. doi: 10.1073/pnas.1511437113. PubMed DOI PMC

Huq E, Quail PH. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 2002;21:2441–2450. doi: 10.1093/emboj/21.10.2441. PubMed DOI PMC

Leivar P, et al. The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell. 2008;20:337–352. doi: 10.1105/tpc.107.052142. PubMed DOI PMC

Hughes RM, Vrana JD, Song J, Tucker CL. Light-dependent, dark-promoted interaction between Arabidopsis cryptochrome 1 and phytochrome B proteins. J. Biol. Chem. 2012;287:22165–22172. doi: 10.1074/jbc.M112.360545. PubMed DOI PMC

Medzihradszky M, et al. Phosphorylation of phytochrome B inhibits light-induced signaling via accelerated dark reversion in Arabidopsis. Plant Cell. 2013;25:535–544. doi: 10.1105/tpc.112.106898. PubMed DOI PMC

Viczian A, et al. Differential phosphorylation of the N-terminal extension regulates phytochrome B signaling. N. Phytol. 2020;225:1635–1650. doi: 10.1111/nph.16243. PubMed DOI

Hornitschek P, et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 2012;71:699–711. doi: 10.1111/j.1365-313X.2012.05033.x. PubMed DOI

Sun J, Qi L, Li Y, Chu J, Li C. PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet. 2012;8:e1002594–e1002594. doi: 10.1371/journal.pgen.1002594. PubMed DOI PMC

Tao Y, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 2008;133:164–176. doi: 10.1016/j.cell.2008.01.049. PubMed DOI PMC

Zheng Z, et al. Local auxin metabolism regulates environment-induced hypocotyl elongation. Nat. Plants. 2016;2:16025. doi: 10.1038/nplants.2016.25. PubMed DOI PMC

Staswick PE, et al. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 2005;17:616–627. doi: 10.1105/tpc.104.026690. PubMed DOI PMC

Jackson RG, et al. Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase. J. Biol. Chem. 2001;276:4350–4356. doi: 10.1074/jbc.M006185200. PubMed DOI

Tanaka K, et al. UGT74D1 catalyzes the glucosylation of 2-oxindole-3-acetic acid in the auxin metabolic pathway in Arabidopsis. Plant Cell Physiol. 2014;55:218–228. doi: 10.1093/pcp/pct173. PubMed DOI PMC

Jin SH, et al. UGT74D1 is a novel auxin glycosyltransferase from Arabidopsis thaliana. PLoS ONE. 2013;8:e61705. doi: 10.1371/journal.pone.0061705. PubMed DOI PMC

Hersch M, et al. Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis. Proc. Natl Acad. Sci. USA. 2014;111:6515–6520. doi: 10.1073/pnas.1320355111. PubMed DOI PMC

Wang R, et al. HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat. Commun. 2016;7:10269. doi: 10.1038/ncomms10269. PubMed DOI PMC

Kadota Y, Shirasu K. The HSP90 complex of plants. Biochim. Biophys. Acta. 2012;1823:689–697. doi: 10.1016/j.bbamcr.2011.09.016. PubMed DOI

Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA. 1998;95:7197–7202. doi: 10.1073/pnas.95.12.7197. PubMed DOI PMC

Spartz AK, et al. The SAUR19 subfamily of Small Auxin UP RNA genes promote cell expansion. Plant J. 2012;70:978–990. doi: 10.1111/j.1365-313X.2012.04946.x. PubMed DOI PMC

Huber, M., Nieuwendijk, N. M., Pantazopoulou, C. K. & Pierik, R. Light signalling shapes plant-plant interactions in dense canopies. Plant Cell Environ.44, 1014–1029 (2021). PubMed PMC

Quint M, et al. Molecular and genetic control of plant thermomorphogenesis. Nat. Plants. 2016;2:15190–15190. doi: 10.1038/nplants.2015.190. PubMed DOI

Zhu Z, Lin C. Photomorphogenesis: when blue meets red. Nat. Plants. 2016;2:16019. doi: 10.1038/nplants.2016.19. PubMed DOI

de Wit M, et al. Integration of phytochrome and cryptochrome signals determines plant growth during competition for light. Curr. Biol. 2016;26:3320–3326. doi: 10.1016/j.cub.2016.10.031. PubMed DOI

Kupers, J. J., Oskam, L. & Pierik, R. Photoreceptors regulate plant developmental plasticity through auxin. Plants9, 940 (2020). PubMed PMC

Wong JH, Spartz AK, Park MY, Du M, Gray WM. Mutation of a conserved motif of PP2C.D phosphatases confers SAUR immunity and constitutive activity. Plant Physiol. 2019;181:353–366. doi: 10.1104/pp.19.00496. PubMed DOI PMC

Takahashi K, Hayashi K, Kinoshita T. Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol. 2012;159:632–641. doi: 10.1104/pp.112.196428. PubMed DOI PMC

Spartz AK, et al. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell. 2014;26:2129–2142. doi: 10.1105/tpc.114.126037. PubMed DOI PMC

Schopfer P. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J. 2001;28:679–688. doi: 10.1046/j.1365-313x.2001.01187.x. PubMed DOI

Schmidt R, Kunkowska AB, Schippers JH. Role of reactive oxygen species during cell expansion in leaves. Plant Physiol. 2016;172:2098–2106. doi: 10.1104/pp.16.00426. PubMed DOI PMC

Ren H, Park MY, Spartz AK, Wong JH, Gray WM. A subset of plasma membrane-localized PP2C.D phosphatases negatively regulate SAUR-mediated cell expansion in Arabidopsis. PLoS Genet. 2018;14:e1007455. doi: 10.1371/journal.pgen.1007455. PubMed DOI PMC

Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 2007;53:312–323. doi: 10.1111/j.1365-313X.2007.03341.x. PubMed DOI

Ahmad M, Lin C, Cashmore AR. Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyl elongation. Plant J. 1995;8:653–658. doi: 10.1046/j.1365-313X.1995.08050653.x. PubMed DOI

Mockler TC, Guo H, Yang H, Duong H, Lin C. Antagonistic actions of Arabidopsis cryptochromes and phytochrome B in the regulation of floral induction. Development. 1999;126:2073–2082. doi: 10.1242/dev.126.10.2073. PubMed DOI

Gray WM, Muskett PR, Chuang HW, Parker JE. Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell. 2003;15:1310–1319. doi: 10.1105/tpc.010884. PubMed DOI PMC

Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 1997;9:1963–1971. PubMed PMC

Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. doi: 10.1046/j.1365-313x.1998.00343.x. PubMed DOI

Schindelin J, et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC

Shinomura T, et al. Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA. 1996;93:8129–8133. doi: 10.1073/pnas.93.15.8129. PubMed DOI PMC

Ori N, Eshed Y, Chuck G, Bowman JL, Hake S. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development. 2000;127:5523–5532. doi: 10.1242/dev.127.24.5523. PubMed DOI

Novak O, Pencik A, Blahousek O, Ljung K. Quantitative auxin metabolite profiling using stable isotope dilution UHPLC-MS/MS. Curr. Protoc. Plant Biol. 2016;1:419–430. doi: 10.1002/cppb.20028. PubMed DOI

Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–169. doi: 10.1093/bioinformatics/btu638. PubMed DOI PMC

Chen Y, Lun AT, Smyth GK. From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res. 2016;5:1438. PubMed PMC

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC

Kaufmann K, et al. Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP) Nat. Protoc. 2010;5:457–472. doi: 10.1038/nprot.2009.244. PubMed DOI

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC

Heinz S, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell. 2010;38:576–589. doi: 10.1016/j.molcel.2010.05.004. PubMed DOI PMC

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. doi: 10.1093/bioinformatics/btq033. PubMed DOI PMC

Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 2013;14:178–192. doi: 10.1093/bib/bbs017. PubMed DOI PMC

Tian T, et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017;45:122–129. doi: 10.1093/nar/gkx382. PubMed DOI PMC