Thermomorphogenesis - Universidad de Costa Ricabiologia.ucr.ac.cr/profesores/Garcia...

PP70CH02_Casal ARjats.cls February 1, 2019 13:28

Annual Review of Plant Biology

ThermomorphogenesisJorge J. Casal1,2 and Sureshkumar Balasubramanian3

1Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA),Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Facultad deAgronomía, Universidad de Buenos Aires, C1417DSE Buenos Aires, Argentina;email: [email protected] de Investigaciones Bioquímicas de Buenos Aires, Consejo Nacional de InvestigacionesCientíficas y Técnicas (CONICET) and Fundación Instituto Leloir, C1405BWE Buenos Aires,Argentina3School of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia;email: [email protected]

Annu. Rev. Plant Biol. 2019. 70:2.1–2.26

The Annual Review of Plant Biology is online atplant.annualreviews.org

https://doi.org/10.1146/annurev-arplant-050718-095919

Copyright © 2019 by Annual Reviews.All rights reserved

Keywords

phytochrome B, PIF4, ELF3, COP1, chromatin remodeling, auxin

Abstract

When exposed to warmer, nonstressful average temperatures, some plantorgans grow and develop at a faster rate without affecting their final di-mensions. Other plant organs show specific changes in morphology ordevelopment in a response termed thermomorphogenesis. Selected cod-ing and noncoding RNA, chromatin features, alternative splicing variants,and signaling proteins change their abundance, localization, and/or intrin-sic activity to mediate thermomorphogenesis. Temperature, light, and cir-cadian clock cues are integrated to impinge on the level or signaling ofhormones such as auxin, brassinosteroids, and gibberellins. The light re-ceptor phytochrome B (phyB) is a temperature sensor, and the phyB–PHYTOCHROME-INTERACTING FACTOR 4 (PIF4)–auxin moduleis only one thread in a complex network that governs temperature sensi-tivity. Thermomorphogenesis offers an avenue to search for climate-smartplants to sustain crop and pasture productivity in the context of global cli-mate change.

2.1Review in Advance first posted on February 20, 2019. (Changes may still occur before final publication.)

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mailto:[email protected]

mailto:[email protected]

https://doi.org/10.1146/annurev-arplant-050718-095919


Contents

1. INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21.1. The Temperature Environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21.2. Definition of Thermomorphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31.3. General and Specific Responses to Average Temperature . . . . . . . . . . . . . . . . . . . . . . 51.4. The Shape of the Response to Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

2. TEMPERATURE SENSING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62.1. Thermodynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62.2. Phytochrome B as a Thermosensor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62.3. Other Sensors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

3. RNA DYNAMICS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84. CHROMATIN REMODELING. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

4.1. H2A.Z Nucleosomal Dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104.2. Histone Deacetylation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104.3. Histone Methylation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

5. ALTERNATIVE SPLICING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115.1. Temperature-Dependent Alternative Splicing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115.2. Alternative Splicing and the Induction of Flowering . . . . . . . . . . . . . . . . . . . . . . . . . . 11

6. PHYTOCHROME-INTERACTING FACTOR 4 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126.1. PHYTOCHROME-INTERACTING FACTOR 4, SHOOT GROWTH,

AND IMMUNITY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126.2. PHYTOCHROME-INTERACTING FACTOR 4 and Flowering . . . . . . . . . . . . 126.3. PHYTOCHROME-INTERACTING FACTOR 4 and Stomata Density . . . . . . 136.4. PHYTOCHROME-INTERACTING FACTOR 4 Expression . . . . . . . . . . . . . . . . . . . 146.5. PHYTOCHROME-INTERACTING FACTOR 4 Stability . . . . . . . . . . . . . . . . . . 156.6. PHYTOCHROME-INTERACTING FACTOR 4 Binding to its Targets . . . . . 156.7. Transcriptional Activity of Bound PHYTOCHROME-INTERACTING

FACTOR 4 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167. HORMONAL REGULATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

7.1. Auxin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177.2. Brassinosteroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187.3. Gibberellins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

8. ECOLOGY OF THERMOMORPHOGENESIS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188.1. Adaptation to Average Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188.2. The Function of Plant Plasticity in Response to Average Temperature . . . . . . . . . 198.3. Crop and Pasture Yield . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

1. INTRODUCTION

1.1. The Temperature Environment

Plants experience a fluctuating thermal environment characterized by average, maximum, andminimum daily temperatures (Figure 1a). These parameters change over the course of the sea-sons, with the summer exhibiting elevated values and amplitudes (i.e., the differences betweenmaximum and minimum temperatures) (Figure 1b). Temperature amplitude is greatest at the sur-face of the soil (which has higher maximum and lower minimum temperatures), and it decreases

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Figure 1

The temperature environment. (a) Temperature parameters and the effects of (b) seasons, (c) temperature-measurement position relative to the soil, and (d) canopy shade are shown over a 24-hour period.

both with deepness in the soil (which also delays the occurrence of maximum and minimum tem-peratures) and with height above soil level (Figure 1c). Shading from neighbors reduces daytimetemperatures, particularly maximum temperatures, with little effect during the night (Figure 1d).These fluctuations affect plant tissue temperature, which depends on the changes caused by thesurrounding air (sensible heat) and soil (heat conduction), absorbed solar radiation and emittedlong-wavelength radiation (radiative transfer), and the heat released by the evaporation of water(latent heat). In addition to these thermal fluctuations, global climate change implies that plantswill also have to face a thermal environment that differs from that experienced by their ancestors.

1.2. Definition of Thermomorphogenesis

Thermomorphogenesis is the effect of temperature on plant morphogenesis (28), i.e., on the or-ganization and shape of the plant body. The term thermomorphogenesis can be traced back toa 1983 paper by Stoller & Woolley (103) describing the effects of alternating temperature and

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light on the formation of basal bulbs in the weed Cyperus esculentus. Similar to photomorphogen-esis, which describes the effects of light cues on growth and development, thermomorphogenesisrefers to the effects of temperature cues (Figure 1) on these processes.

We can group thermomorphogenesis responses into three types, depending on whether the ef-fective parameters that optimize the output are cold average temperatures, rhythmic thermal fluc-tuations, or warm average temperatures (Figure 2a). The first type includes vernalization (4)—oracceleration of flowering by prolonged periods (weeks) of low temperatures—and stratification(113)—or promotion of seed germination by moist chilling. The second type, termed thermope-riodism, includes responses, such as seed germination (109) and stem growth (7), which oftenrequire alternating (day/night) temperatures. The third type of thermomorphogenesis response,which looks at the effects of mild, warm average temperature on plant growth and development,

Temperaturecue:

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Figure 2

Thermomorphogenesis. (a) Induction of growth and developmental responses by different temperature cues. (b) Kinetics of the generaland specific effects of average temperature on growth (top) and developmental timing (bottom). Note that general effects alter only therate, whereas specific responses affect the end point. (c) Specific morphological and developmental responses to average temperature.Arabidopsis thaliana seedlings of the Columbia background were grown under short days at 23°C and 27°C. Note that warmtemperatures enhance the growth of the hypocotyl and petioles but not the growth of the cotyledons or leaf lamina (top) and that plantsexposed to warm temperatures flower early (bottom, shown at four weeks) while the cooler-temperature controls continue producingleaves (inset, shown at seven weeks).


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is the focus of this review, and the other two are not further addressed here. The indirect mor-phological effects derived from the stress caused by temperature extremes (e.g., heat shock or coldshock) and the biochemical acclimation to these extremes without a correlate on plant form arenot considered thermomorphogenesis.

1.3. General and Specific Responses to Average Temperature

Not every growth or developmental response to warm temperature is thermomorphogenesis.There are general responses, where higher average temperatures accelerate growth and devel-opment but leave the final body shape unaffected. Warm temperatures can increase the rate ofgrowth of a given organ and proportionally decrease its growth duration by accelerating the rateof developmental progression (Figure 2b). Developmental events can occur faster with increas-ing temperatures while maintaining their coordination (Figure 2b). In Arabidopsis thaliana, therate but not the final percentage of seed germination increases between 7°C and 13–28°C (46),and the rates of seed germination, leaf appearance, and leaf expansion show coordinated responsesto temperature (80).

Thermomorphogenesis involves specific responses, where warm temperatures do more thansimply accelerate growth because different temperatures are found to affect the final plant mor-phologies (Figure 2b). In A. thaliana, hypocotyl growth is much faster at 29°C than at 20°C butceases simultaneously at both temperatures (39). The resulting differences in hypocotyl lengthindicate that there is a specific effect of warm temperature on growth. Although the hypocotyland the leaf petiole exhibit greater growth under warm temperatures, the cotyledons and the leaflamina do not show much variation (Figure 2c), indicating organ-specific effects. Warm temper-atures also induce hyponasty, which elevates the position of the leaves by increasing the angle ofthe petioles because the abaxial face of the petiole has grown faster than the adaxial face. The ra-tio between leaf-lamina length and width may also increase with temperature, resulting in a moreelongated leaf shape (50). Warm temperatures also reduce the stomatal index, which is the ratiobetween stomatal and epidermal cells (60). The primary root becomes longer but narrower withwarmer temperatures (42, 114, 118). In A. thaliana accessions that do not require vernalization, atemperature increase from 16°C to 28°C accelerates flowering time much more than the rate ofleaf production, and this decreases the number of leaves at flowering (2, 5, 41, 52, 73) (Figure 2b,c).

1.4. The Shape of the Response to Temperature

Diverse responses to warm temperature are unimodal, with rates that show an initial increase,a transition, and a final decrease (25). Within the rising phase, the relationship between growthrates or developmental rates and temperature is approximately linear between base and optimumtemperatures (98). This has given rise to the concept of thermal time (110). The progression ofthermal time depends on the daily temperature accumulation above the base temperature (i.e., thedaily average temperature minus the base temperature in degree days).The expression of develop-mental phase duration in units of thermal time (degree days) is of wide applicability in agriculture,because this duration can be converted to chronological units (days) by using the particular tem-perature patterns of a given location or year in order to predict the date of occurrence of keyevents. General effects of temperature on growth or development (Figure 2b) disappear when ki-netics are plotted against accumulated thermal time rather than accumulated chronological time,but specific effects of temperature (Figure 2b) still persist (e.g., at a given accumulated thermaltime the stem can be taller if the plants were grown at a warmer temperature).


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Phytochrome B(phyB): aphotosensory receptorbearing an open-chaintetrapyrrolechromophore that isalso able to sensetemperature

Table 1 Molecular and cellular events in thermomorphogenesis

Regulated process ExamplesChromatin remodeling H2A.Z nucleosome occupancy, H3K9 acetylation at nucleosomes, histone H3 methylationAlternative splicing FLMIsomerization phyB (Pfr-to-Pr reversion)Dimerization UVR8Gene expression PIF4, YUC8, TAA1, CYP79B2, Aux/IAAs,GH3s, SAURs,HSP70, PR1, PR5, SPCH,HY5,

HFR1, LNGs, CPD,DWF4,GA20ox1,GA3ox1Noncoding RNA expression miR169,miR172, FLINCProtein degradation PIF4, HY5, DELLAs, HFR1Subcellular localization COP1, phyB, BZR1Association to DNA ELF3, phyB, PIF4, cry1Hormone accumulation Auxin

Abbreviations: Aux/IAA, auxin/indole-3-acetic acid; BZR1, BRASSINAZOLE-RESISTANT 1; COP1, CONSTITUTIVE PHOTOMORPHOGENIC 1;CPD, CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARFISM; cry1, cryptochrome 1; CYP79B2, CYTOCHROME P450 FAMILY 79B; DWF4,DWARF4; ELF3, EARLY FLOWERING 3; FLINC, FLOWERING LONG INTERGENIC NONCODING RNA; FLM, FLOWERING LOCUS M;GA20ox1, gibberellin 20-oxidase 1; GA3ox1, gibberellin 3-beta-dioxygenase 1; GH3, GRETCHEN HAGEN 3; HFR1, LONG HYPOCOTYL IN FAR RED 1;HSP70,HEAT SHOCK PROTEIN 70; HY5, LONG HYPOCOTYL 5; LNGs, LONGIFOLIAs; Pfr, far-red light–absorbing phytochrome; phyB,phytochrome B; PIF4, PHYTOCHROME-INTERACTING FACTOR 4; Pr, red light–absorbing phytochrome; PR1/5, PATHOGENESIS-RELATED GENE1/5; SAURs, SMALL AUXIN UP RNAs; SPCH, SPEECHLESS; TAA1, TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1; UVR8,UV-RESISTANCE LOCUS 8; YUC8, YUCCA 8.

2. TEMPERATURE SENSING

2.1. Thermodynamics

The rising part of the response to temperature can be interpreted using the Boltzmann–Arrheniusmodel, according to which (a) the occurrence of a reaction requires that the substrates achieve theenthalpy of activation or activation energy and (b) the proportion of molecules in the active stageincreases with temperature (25, 98). This thermodynamic model is conceptually based on a singlebiochemical reaction limiting the overall rate of complex biological process (a rather unlikelyscenario), but it is also compatible with the occurrence of multiple reactions controlling the rateacross the temperature-response range (98).

General responses to average temperature could result from a system-level adaptation, whererate-limiting components share similar thermodynamic patterns. In specific responses, the ther-mosensors show a differential response. Diverse molecular and supramolecular structures canchange their activity with temperature, and any of them could be thermosensory receptors(15). Several molecular and cellular processes are affected by average temperature in A. thaliana(Table 1). However, the sensor has to be the primum movens, and the observed changes may wellbe downstream effects.

2.2. Phytochrome B as a Thermosensor

The photosensory receptor phytochrome B (phyB) has been identified as a temperature sensor(53, 64). Phytochromes have two photo-interconvertible forms (11). They are synthesized in thered light–absorbing form (Pr) that is photo-transformed to the far-red light–absorbing form (Pfr)upon exposure to red light. In turn, Pfr is photo-transformed to Pr by far-red light. Phytochromesare head-to-head dimers in vivo and the Pfr–Pfr homodimer is considered the active conformerof phyB (55). In addition to the Pr-to-Pfr and Pfr-to-Pr photo-chemical reactions, the Pfr formcan back-revert to Pr via thermal reversion (Figure 3), a reaction that does not require light and


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Pr PfrPr Pr Pfr Pfr

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Figure 3

Temperature and light sensing by phyB. The steady state of the active conformer of phyB, the Pfr–Pfrhomodimer, depends on light and thermal reactions. Abbreviations: Pfr, far-red light–absorbingphytochrome; phyB, phytochrome B; Pr, red light–absorbing phytochrome.

for this reason is also termed dark reversion. It is important to distinguish between reversioneither from Pfr–Pfr to Pfr–Pr or from Pfr–Pr to Pr–Pr. The second reaction is tenfold faster,indicating that when Pfr is dimerized to Pr it becomes considerably less stable (55). Both ratesof Pfr-to-Pr reversion significantly increase with temperature within the physiological range (0–30°C) (53, 64). Photoconversion and reversion of phyB are affected by allosteric features proximaland distal to the bilin chromophore (10).The proportion of phyB as Pfr–Pfr homodimers increaseswith the red/far-red ratio of the light and decreases with temperature because red light drivesthe Pr-to-Pfr photochemical reaction, while far-red light and warm temperatures drive the Pfr-to-Pr photochemical and thermal reactions, respectively (65). Thermal reversion increases theirradiance dependency of the system because more light is required to achieve a given level ofPfr if it becomes thermally unstable. Therefore, phyB provides information about the presenceof neighboring vegetation, which reduces the red/far-red ratio (red light is strongly absorbed byphotosynthetic pigments, while green tissues reflect and transmit most of the far-red light) andirradiance (canopy shade), and information about tissue temperature (Figure 3). Not only lightbut also temperature affects the dynamics of in vitro–synthesized phyB (64), indicating that phyBis a primum movens because temperature-induced changes in phyB activity do not require othercomponents of the system.

Thermal reversion is the main driver of temperature effects on phyB activity, and available in-formation does not demonstrate significant effects of temperature on the steady-state level of totalor nuclear phyB (53, 64). These changes in phyB activity impact on hypocotyl growth, indicatingthat phyB partially mediates the physiological output in response to different temperatures (64).phyB is one of the sensors that mediate specific morphological responses to temperature but notgeneral responses. For instance, the rate of leaf appearance is accelerated by warm temperaturesand slowed down by the phyBmutation (74). Temperature modifies the formation of phyB nuclearbodies and the (indirect) association of phyB to DNA (53, 64). These effects derive in part fromthe modified activity, but the rates of association and dissociation could also be directly affectedby temperature.


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Thermal reversion of phyB can be modulated by biochemical modifications, such as phospho-rylation (75), or interaction with binding partners, including PHOTOPERIODIC CONTROLOF HYPOCOTYL 1 (PCH1) and its homolog, PCH1-LIKE (PCHL) (27). PCH1 and PCHLphysically interact with active phyB and reduce its rate of thermal reversion.

2.3. Other Sensors

Because the phyBmutant retains a thermomorphogenic response, there must be other entry portsfor the temperature cue. Phytochromes are a family of photosensory receptors encoded by fivegenes in A. thaliana. Hypocotyl growth (53) and flowering (92) responses to temperature presentin phyB are lost in the quintuple phytochrome mutant, which indicates that other phytochromeseither also sense temperature or are at least necessary to establish the conditions for a temper-ature response. In A. thaliana, no thermal reversion has been observed for phyA. However, thishas been analyzed under conditions dominated by the Pfr–Pfr-to-Pfr–Pr reversion and whetherthe same is true for the Pfr–Pr-to-Pr–Pr reversion remains to be elucidated. It is noteworthythat evidence for temperature-dependent phyA Pfr-to-Pr reversion has been obtained in squash(93).

In the liverwort Marchantia polymorpha, it has been found that the blue-light photoreceptorphototropin is also able to sense temperature because warm temperatures reduce the lifetimeof the light-activated receptor (35). Under strong blue light, the chloroplasts of M. polymorphamove to the periphery of the cell to avoid the damage caused by excessive light. However, at lowtemperatures, weaker light can still be damaging because enzymes of the Calvin cycle are slowto process the products of the light reactions of photosynthesis. Under low-temperature, weak-light conditions, chloroplast intracellular relocation is induced by the weak-light activation ofphototropin combined with its extended lifetime under low temperatures.

The use of photosensory receptors to sense temperature is present from bacteria through plantsand animals (15).Mechanistically, this is based on the fact that light activates photosensory recep-tors that then return to their ground state via a reaction that does not require light, thus accom-modating the temperature input.The role of phototropins in thermomorphogenesis ofA. thalianaremains to be established. Although mutations or allelic variation in the blue-light receptors cryp-tochromes have also been shown to modulate temperature sensitivity in A. thaliana, it is currentlyunclear whether they are involved in sensing (70, 91). Although photosensory receptors other thanphyB are very good candidates as additional temperature sensors (15, 65), there is evidence for arole of thermometers not involved in light sensing. For instance, hypocotyl growth responds totemperature in the phyB mutant transferred to darkness after a pulse of far-red light; i.e., under acondition where all the photosensory receptors are predicted to be inactive (64).

3. RNA DYNAMICS

Many genes show a faster rate of transcription at 27°C than at 17°C, but this is compensated by afaster rate of degradation, with average temperature coefficients (Q10, the factor by which the rateof a reaction increases for every 10-degree rise in temperature) of 3.6 and 3.3, respectively (99).A relatively small proportion of the genes increase or decrease their steady-state levels by havingrespectively larger or smaller temperature coefficients than the average but no significant biasin the decay response (99). There is limited overlap among differentially expressed genes fromthe several studies describing transcriptome responses to temperature (12, 19, 79). Within theset of genes with consistent responses to temperature in these studies (Supplemental Table 1),in addition to response to temperature stimulus, other overrepresented Gene Ontology terms


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H2A.Z: a variant ofhistone H2A, whichreplaces theconventional H2A insome nucleosomes

include response to light stimulus, response to hormone stimulus, and response to jasmonic acidstimulus as well as flavonoid biosynthetic processes.

Temperature affects the steady-state levels of only a small fraction of the small RNAs (21–24nucleotides) (40) and long noncoding RNAs in A. thaliana (97). Warm temperatures reduce theexpression ofmicroRNA 169 (miR169), which targets the messenger RNA (mRNA) of NUCLEARFACTOR Y (NF-Y) complex genes involved in the promotion of flowering (40, 62, 96). Warmtemperatures also enhance the expression of miR172, and overexpression of miR172 in trans-genic seedlings causes temperature-independent early flowering (62). A temperature-dependentgrowth defect associated with triplet repeat expansions has been shown to be mediated through atemperature-dependent increase in 24-nucleotide small RNAs (26). Among the long noncodingRNAs, FLOWERING LONG INTERGENIC NONCODING RNA (FLINC) showed decreased ex-pression at 25°C and the mutant flowered early, particularly at 16°C, which suggests that FLINChas a role in thermomorphogenesis (97).

4. CHROMATIN REMODELING

One of the primary events in the regulation of transcription is the unpacking of the DNAwrappedaround the nucleosomes. Warm average temperatures lead to both histone modifications and areduction in occupancy of H2A.Z, which is one of the histone variants (Figure 4). The molecularevents associated with the observed reduction in H2A.Z in response to high temperature are notunderstood with the same level of detail as those taking place during vernalization (4), and thethermosensing steps upstream of chromatin remodeling are currently unknown.

H2BH2A

H4

H2B

H4H3

H2A.Z

Ac

K9K9

Me Me

K36K36

Ac

PWR/HDA9

complex

ARP6

H3

Transcription

Positive regulation

Negative regulation

RNA

DNA

Figure 4

Chromatin dynamics in thermomorphogenesis. Transcriptionally permissive (left) and transcriptionallyrepressive (right) nucleosome states. The elements represented in red increase under warm temperatures,whereas those elements represented in blue increase under cooler temperatures. Abbreviations: Ac,acetylation; ARP6, ACTIN-RELATED PROTEIN 6; HDA9, HISTONE DEACETYLASE 9; Me,methylation; PWR, POWERDRESS.


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POWERDRESS(PWR): a protein thatinteracts withHISTONEDEACETYLASE 9 todecrease the level ofacetylation of histone 3

HISTONEDEACETYLASE 9(HDA9): a proteinthat interacts withPOWERDRESS todecrease the level ofacetylation of histone 3

4.1. H2A.Z Nucleosomal Dynamics

Two mutant actin-related protein 6 (arp6) alleles were identified in a screen for A. thaliana seedlingswith altered expression of HEAT SHOCK PROTEIN 70 (HSP70) (58), a warm temperature–induced gene (2, 58). The arp6 mutants displayed high HSP70 promoter activity, high expressionof other warm temperature–induced genes, early flowering, long hypocotyls at low temperature,reduced expression of warm temperature–repressed genes, and attenuated responses to tempera-ture (58).ARP6 encodes a member of the SWR1 protein complex that deposits onto nucleosomesthe histone H2A.Z variant rather than histone H2A. A double mutant of genes encoding H2A.Zalso showed elevatedHSP70 expression, early flowering, and long hypocotyls (58). In a particularlynoteworthy finding, there is a high H2A.Z occupancy of the first nucleosome downstream of thetranscription start site (+1 nucleosome) at lower temperatures that is strongly and rapidly reducedwhen the plants are transferred to warmer conditions (19, 58) (Figure 4). These observations areconsistent with a model where warm temperature–induced eviction of H2A.Z-containing nucle-osomes helps to unwrap DNA and allows access to transcriptional regulators that either activateor repress gene expression in response to high temperature (58). Eviction of H2A.Z-containingnucleosomes is unlikely to be specific for the response to high temperature: Genome-wide studiesindicate that the presence of H2A.Z in gene bodies correlates with lower basal expression levelsand with the high responsiveness of these genes to developmental context and multiple environ-mental cues. Conversely, genes where DNA methylation excludes H2A.Z in gene bodies tend tohave more stable expression (18).

When purified from A. thaliana seedlings grown at 17°C, the H2A.Z nucleosomes at the +1position of HSP70 do not show eviction in response to an in vitro temperature shift to 27°C(19). This indicates that the nucleosomes are not intrinsically sensing the temperature cue but areaffected by upstream temperature-induced changes that could involve transcription factors and/orremodelers. The binding of the transcription factor HEAT SHOCK FACTOR 1A (HSF1A) tothe genes that respond to nonstressful warm temperatures is significant at low temperatures andincreases with warmth (19). Rapid gene expression–responses to warm temperature require bothHSFA1 class transcription factors and H2A.Z nucleosomes (19). The +1 H2A.Z nucleosome atthe HSP70 gene fails to respond to temperature changes in a quadruple mutant of HSFA1 classtranscription factors (19). HSF1A transcription factors can convey temperature information totheir targets and while they have a well-documented role in acclimation to temperature stress(19), their function in thermomorphogenesis remains to be elucidated.

4.2. Histone Deacetylation

The powerdress (pwr) mutant was identified in a screen for A. thaliana seedlings with reduced ther-mal response of hypocotyl elongation. It shows attenuated petiole growth, flowering, and tran-scriptome responses to temperature changes (106). PWR bears a domain typically involved in theregulation of the interaction between histone tails and the histone-modifying enzymes. Inhibitorsof histone deacetylation impaired the growth response of the hypocotyl, whereas inhibitors of hi-stone acetylation had no effect (106). The latter finding indicates a role for histone deacetylationin thermomorphogenesis, and this is further supported by the physical interaction between PWRand HISTONE DEACETYLASE 9 (HDA9) (17, 54) and the observation of severely attenuatedresponses to temperature in the hda9mutant (106).Warm temperatures induce a strong reductionof H3K9 acetylation at the +1 nucleosomes of genes that respond to temperature in the wild type(Figure 4), while the pwr mutant exhibits H3K9 hyperacetylation (59).

A contradiction that remains to be explained is that deacetylation is typically associated witha reduction in gene expression, whereas the pwr mutant shows hyperacetylation and reduced


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FLOWERINGLOCUS M (FLM):a MADS-boxtranscription factorthat repressesflowering

induction of expression of warm temperature–induced genes (106). One possibility is that histoneH3 deacetylation mediated by PWR/HDA9 induces eviction of H2A.Z from the nucleosomes andindirectly enhances gene expression. In favor of this interpretation, nucleosomal dynamics and hi-stone deacetylation are two distinct chromatin-remodeling events that appear to be linked in theresponse to temperature; there is significant overlap between the genes with expression affectedby mutants in genes involved in these processes (106).

4.3. Histone Methylation

Another biochemical modification apparently important in thermomorphogenesis is histonemethylation (Figure 4). Histone H3 lysine 36 trimethylation (H3K36me3) levels tend to behigher and H3K36me3 regions tend to be broader at 25°C than at 16°C (79). Mutations atH3K36me3 writers, erasers, or readers (modulator proteins that add, remove, or recognize thesemodifications, respectively) impair the flowering response to temperature in A. thaliana, appar-ently by affecting alternative splicing (79). The presence of the H3K27me3 marks correlates withgenes having either high or low transcription rates under warm temperatures (99). It is possi-ble that H3K27me3 marks are present in a subset of H2A.Z-containing genes and that H2A.Zpresence in gene bodies together with H3K27me3 contributes to a reduced rate of transcrip-tion (14, 99). H3K4me2 is transiently elevated at selected regions of the promoters in somewarm temperature–induced genes and subsequently demethylated in a process that involves theFLOWERINGCONTROL LOCUS A (FCA) protein and affects the pattern of gene expression(61).

5. ALTERNATIVE SPLICING

5.1. Temperature-Dependent Alternative Splicing

One of the earliest links between alternative splicing and temperature came through the analysis ofthe temperature-sensitive splicing allele apetala3-1, which affects floral organ identity (90, 115). Atranscriptome-wide analysis identified 683 events of temperature-induced differential splicing inplants shifted from 16°C to 25°C, which derive from 511 distinct genes in A. thaliana (79). Thereis little overlap between the genes showing differential splicing and differential expression in re-sponse to temperature, indicating that these are largely alternative pathways to control the levelsof specific transcripts (79). Analysis of the knockout lines for differentially expressed genes thatare associated with splicing identified PORCUPINE (PCP), a gene encoding a small ribonuclearprotein, as having reduced expression at warm temperatures. Mutations in PCP led to a pheno-type manifested only at low temperatures, which suggests that PCP may be important to controlsplicing at low temperatures (12).

5.2. Alternative Splicing and the Induction of Flowering

FLOWERING LOCUS M/MADS-ASSOCIATED WITH FLOWERING 1 (FLM/MAF1) is aMADS-box transcription factor that represses the expression of FLOWERING LOCUS T (FT)and is implicated in thermal induction of flowering in A. thaliana (2, 3). FLM produces differ-ent splicing variants (95), and genome-wide analysis of the shoot-apex transcriptome revealedtemperature-induced changes in the expression of RNA processing factors, leading to the ideathat elevated temperatures could modify the alternative splicing of FLM and reduce the variantthat represses flowering (2, 3).


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PHYTOCHROME-INTERACTINGFACTOR 4 (PIF4):a transcription factorinvolved in theintegration of differentstimuli

YUCCA 8 (YUC8):an enzyme involved inthe control of auxinsynthesis

An earlier proposal to account for the regulation of FLM activity by alternative splicing wasbased on two splicing isoforms, FLM-beta and FLM-delta, which compete for an interaction part-ner, the flowering repressor SHORT VEGETATIVE PHASE (SVP) (83). The FLM-beta com-plex would predominate in the cold, whereas the SVP–FLM-delta complex would increase withwarm temperature (83). Since the SVP–FLM-delta complex has reduced DNA-binding capacity,this would result in a release of FT expression from the inhibition imposed by SVP in response tohigh temperature (83). According to this model, the effect of FLM would depend on the balanceof its isoforms acting in opposite directions. However, this idea has failed to stand the test of time:There is no consistent increase in the FLM-delta splice variant with high temperature, and thisisoform does not appear to be functionally relevant (105). Rather,most of the phenotypic effects ofFLM can be explained by the levels of functional FLM-beta variant, which decreases in the warmth(13, 68, 69). It turns out that FLM has several temperature-sensitive splice sites that give rise tomultiple splice variants. Higher temperatures increase the proportion of FLM transcripts that aretargeted by the nonsense-mediated mRNA decay pathway, and this results in a downregulation ofFLM expression and early flowering (105).

6. PHYTOCHROME-INTERACTING FACTOR 4

6.1. PHYTOCHROME-INTERACTING FACTOR 4, SHOOT GROWTH,AND IMMUNITY

The helix–loop–helix transcription factor PHYTOCHROME-INTERACTING FACTOR 4(PIF4) has a fundamental role in shoot thermomorphogenesis in A. thaliana.Warm temperature–induced hypocotyl growth, petiole growth, and leaf hyponasty depend on PIF4, with a contri-bution from PIF5 (56, 102). PIF4 mediates vegetative shoot thermomorphogenesis by virtueof its capacity to bind the promoters of genes involved in auxin synthesis, including YUCCA 8(YUC8) (104), TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1), andCYTOCHROME P450 FAMILY 79B (CYP79B2) (33) (Figure 5; see also Section 7.1).While pro-moting vegetative growth, PIF4 represses immunity.The expression of defense-related genes suchas PATHOGENESIS-RELATED GENE 1 (PR1) and PR5 is reduced by warm temperatures in thewild type but remains constitutively high in the pif4 mutant, suggesting that PIF4 could mediatethe trade-off between growth and immunity (37).

PIF4 also binds the E-box motif variant CACATG, which is present in the promoters of theLONGIFOLIA1 (LNG1) and LNG2 genes and increases their expression at warm temperatures(50). A quadruple lng1 lng2 lng3 lng4 mutant showed attenuated responses to temperature inhypocotyl and petiole growth, leaf lamina shape, and PIF4 target gene expression (50). LNG1and LNG2 may be part of a feed-forward loop increasing the transcriptional activity of PIF4without affecting PIF4 gene expression or PIF4 protein abundance (50).

6.2. PHYTOCHROME-INTERACTING FACTOR 4 and Flowering

The binding of PIF4 to the FT promoter increases at 27°C, compared with 22°C or 12°C(Figure 5), and is apparently facilitated by a temperature-induced reduction of H2A.Z nucleo-some occupancy (57). In A. thaliana plants grown under short days, there is warm temperature–induced accumulation of FT and its paralog,TWIN SISTER OF FT (TSF), at dusk, which dependson PIF4, PIF5, CONSTANS (CO), and physical interaction between CO and PIF4 (30). How-ever, although an early study reported late flowering of the pif4mutant exposed to warm temper-atures under short days and early flowering of PIF4 overexpressors at intermediate temperatures


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Stomatadevelopment

FloweringStem growth

Transcriptionaltargets

Positive regulation

Negative regulation

mRNA

NucleosomeNucleosomeoooouucleosomecleosomeNuclNucl

NucleosomeNucleosomeoooouucleosomecleosomeNuclNuclCOP1ELF3

BZR1

HY5

PIF4

TAA1, YUC8, CYP79B2, LNG1, LNG2

SPCHFT

HFR1

RGA

PIF4

phyBELF3

HY5

BZR1

FCA

Ac

Transcriptional regulators Posttranscriptional regulators

H2A.Z

Figure 5

The PIF4 network in thermomorphogenesis. Only the links with PIF4 are included. The elementsrepresented in red increase their activity with warm temperatures, whereas those elements represented inblue increase their activity with cooler temperatures. Not all of the transcriptional regulators (left) orposttranscriptional regulators (right) are important in the context of each one of the represented PIF4targets (below). Abbreviations: Ac, acetylation; BZR1, BRASSINAZOLE-RESISTANT 1; COP1,CONSTITUTIVE PHOTOMORPHOGENIC 1; CYP79B2, CYTOCHROME P450 FAMILY 79B; ELF3,EARLY FLOWERING 3; FCA, FLOWERING CONTROL LOCUS A; FT, FLOWERING LOCUS T;HFR1, LONG HYPOCOTYL IN FAR RED 1; HY5, LONG HYPOCOTYL 5; LNG, LONGIFOLIA;phyB, phytochrome B; PIF4, PHYTOCHROME-INTERACTING FACTOR 4; RGA, REPRESSOR OFga1-3; SPCH, SPEECHLESS; TAA1, TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1;YUC8, YUCCA 8.

suppressed by the ft mutation (57), subsequent work from several laboratories indicated that thepif4mutant is only slightly late flowering (30, 105). Furthermore, the flm pif4 double mutant flow-ers early at high temperatures, suggesting that warm temperature–induced derepression (2, 3,105) may be more critical than PIF4-mediated activation in conferring thermosensory floweringresponse.

6.3. PHYTOCHROME-INTERACTING FACTOR 4 and Stomata Density

In A. thaliana, warm temperatures reduce stomatal index by lowering the number of cells express-ing SPEECHLESS (SPCH) (Figure 5), a transcription factor that triggers the initiation of thestomatal lineage, and accumulating the SPCHprotein (60).The pif4mutant shows a high stomatal


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EARLYFLOWERING 3(ELF3):a transcriptionalregulator that is acomponent of theEVENINGCOMPLEX

BRASSINAZOLE-RESISTANT 1(BZR1):a transcription factorinvolved inbrassinosteroidsignaling

CONSTITUTIVEPHOTOMOR-PHOGENIC 1(COP1): an E3 ligaseinvolved in proteinubiquitination andtargeting todegradation

index that fails to decrease in response to a shift from 22°C to 28°C but retains responsivity tolower temperatures (60). At high temperature, PIF4 accumulates in stomatal precursor cells andat E-boxes of the SPCH promoter, which has the effect of reducing the expression of SPCH (60).

6.4. PHYTOCHROME-INTERACTING FACTOR 4 Expression

Transfer to warm temperatures transiently elevates PIF4 expression in whole A. thaliana seedlingsand cotyledons (56, 102) and more stably elevates PIF4 and PIF5 expression in the hypocotyl (102)(Figure 5). Reduced phyB activity caused by shade does not typically elevate PIF4 expression (84),and, therefore, temperature control of PIF4 expression is likely to involve pathways that are notmediated by phyB sensing of the temperature cue. The pwr mutant shows normal expressionof PIF4 and its target YUC8 at 23°C but attenuated response at 27°C, suggesting that histonedeacetylation may be important for PIF4 induction (106).

EARLY FLOWERING 3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX) form theEVENING COMPLEX, which is part of the circadian clock. This complex binds the PIF4 (andPIF5) promoter and represses its expression, particularly during the early portion of the night (77).Therefore, the elf3 mutant has long hypocotyls with poor response to temperature (107) becauseof its high expression levels of PIF4 and PIF5 (77), which confer a phenotype typical of warmconditions even under low temperatures.Warm temperatures attenuate the binding of ELF3 andLUX to their target promoters, contributing to the elevated expression of PIF4 under these con-ditions (8, 29, 86). Although phyB colocalizes with the EVENING COMPLEX at many loci, theeffects of the elf3 and phyB phyD phyE mutations on hypocotyl growth are additive, suggestingparallel temperature pathways for phyB and ELF3 (29).

PIF4 is a direct target of LONG HYPOCOTYL 5 (HY5), which negatively regulates PIF4expression (24, 63), although there are cases where this effect is not evident (38). In addition toits control by visible light and UV-B radiation (59), the expression of the HY5 gene and in somecases the stability of HY5 decrease with increasing temperatures (16, 24, 108).

UV-B radiation perceived by the UV-RESISTANCE LOCUS 8 (UVR8) photosensory recep-tor also reduces PIF4 expression and hence PIF4-mediated gene expression under warm temper-atures (44). UVR8 exists as an inactive dimer, which, in response to UV-B, becomes a monomerable to interact with downstream transduction partners (45). The proportion of UVR8 present asa monomer decreases with temperature, which causes faster reversion to the dimer state (31).

BRASSINAZOLE-RESISTANT 1 (BZR1) is a key transcription factor in brassinosteroid sig-naling,which directly binds thePIF4 promoter, particularly in response to warm temperatures, andactivates its expression (51). Warm temperature–induced hypocotyl growth requires both PIF4and BZR1 (78). Gain-of-function bzr1 mutants or transgenic, overexpressing lines of BZR1 haveenhanced hypocotyl growth and SMALL AUXIN UP RNAs 19 (SAUR19) expression under warmtemperature (51). Warm temperatures increase the nuclear localization of BZR1 without havingsignificant effects on the expression of the BZR1 gene or rapid effects on the abundance of theBZR1 protein (51, 102).

CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) is a RING E3 ligase that formsa complex with SUPPRESSOR OF PHYA-105 1 (SPA1), SPA2, SPA3, and/or SPA4, and thiscomplex acts as a substrate adaptor for a multimeric CULLIN 4 (CUL4)-DAMAGED DNA-BINDING PROTEIN 1 (DDB1) E3 ligase that targets proteins for degradation in the protea-some (59). DE-ETIOLATED 1 (DET1) and COP10 form a different multimeric CUL4–DDB1ligase that apparently reinforces activity of the CUL4–DDB–COP1–SPA multimeric complex(59). The cop1, det1, cop10, cul4, and spa1 spa3 spa4 mutants show reduced hypocotyl growth re-sponses to warm temperatures (24). Warm temperature increases nuclear accumulation of COP1


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DELLA:a protein family oftranscriptionalregulators that repressgene expressionresponses induced bygibberellins

(81). In turn, COP1 and DET1 increase the expression of PIF4, apparently not by reducing HY5(38), despite the fact that HY5 is one of the targets of COP1 (59).

6.5. PHYTOCHROME-INTERACTING FACTOR 4 Stability

In A. thaliana seedlings grown under white light/dark cycles, when the activity of phyB is reducedby shade, PIF4 protein levels increase during the first hours and then follow a tissue-specific dy-namic without significant changes in mRNA levels. This suggests that shade increases PIF4 sta-bility (84). The stability of PIF5 also increases rapidly in response to shade-induced reductions inphyB activity (67). We would therefore expect PIF4 to increase its stability in response to warmtemperatures because the latter also reduce phyB activity. This is indeed the case in seedlingsgrown at 25°C compared with those grown at 15°C under red light/dark cycles (32) (Figure 5).The differences are smaller under blue light/dark cycles (32), which are not as efficient as thecycles with red light to activate phyB. However, no differences in PIF4 stability between 20°Cor 28/29°C were observed for seedlings grown either under continuous white light (102) or un-der long days (16 h of light/8 h of darkness) of white light (44). Under red-light cycles, PIF4accumulates a phosphorylated form (32). During the exposure of dark-grown seedlings to light,active phyB physically interacts with PIF4, facilitating its phosphorylation and degradation in theproteasome (67).However, close inspection of published data reveals the accumulation of slowmi-grating PIF5 (65, figure 5) or PIF4 (79, figure 3d) bands (which might be phosphorylated) whenlight-grown seedlings are exposed to simulated shade. Therefore, there is a correlation betweenthe changes reported for PIF4 when phyB activity is reduced by shade or warmth.

BLADE-ON-PETIOLE 1 (BOP1) and BOP2 are Bric-à-brac/Tramtrack/Broad (BTB) pro-teins that serve as target-recognition adaptors in a CUL3 E3 ligase complex involved in the degra-dation of PIF4 (116). They physically interact with CUL3 and with PIF4 and the CUL3–BOPcomplex mediates the polyubiquitination of PIF4 (116). The bop1 and bop2 mutations additivelyincrease the hypocotyl growth response to warm temperatures, and the pif4 mutation is partiallyepistatic over the bop1 bop2 double mutant (116). The bop1 and bop2 mutants have elevated levelsof PIF4. However, at least bop2 retains significant responses to temperature (116), and it is notclear whether temperature affects the interaction between BOP1 or BOP2 and PIF4.

PIF4 physically interacts with DELLA proteins (22). This interaction is known to reduce thestability of the PIF4 protein (66), but the relevant E3 ligase remains to be established. AlthoughDELLA proteins become unstable under warm temperatures (102), the implications of DELLA-facilitated degradation of PIF4 for the regulation of PIF4 abundance in response to temperaturehave not been elucidated. The det1 or cop1 mutations reduce the rate of hypocotyl growth and itsresponse to temperature in PIF4 overexpressors presumably by reducing PIF4 abundance. Thissupports positive roles for DET1 and COP1 in the control of PIF4 stability (38).

6.6. PHYTOCHROME-INTERACTING FACTOR 4 Binding to its Targets

In addition to the aforementioned effect on PIF4 stability, DELLAs physically interact with theDNA-binding domain of PIF4, sequestering PIF4, which becomes unable to bind its targets (22)(Figure 5). DELLA proteins are degraded in response to gibberellins. Therefore, the promotionof hypocotyl growth by warm temperatures can be reduced by the application of a gibberellin syn-thesis inhibitor (an effect that is reversed by the application of gibberellins), by mutations at gib-berellin synthesis and in gibberellin receptor genes, or by gain-of-function mutations that renderDELLA proteins insensitive to gibberellin (102). All of these conditions increase the abundanceof DELLA and impair the ability of PIF4 to promote hypocotyl growth. Conversely, transfer towarm temperatures reduces the abundance of DELLA in the hypocotyl (102).


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LONG HYPOCOTYL IN FAR RED 1 (HFR1) (48) and PHYTOCHROME RAPIDLYREGULATED 1 (PAR1) (89) are atypical basic helix-loop-helix (bHLH) proteins that form het-erodimers with PIF4, which do not bind to DNA to activate gene expression.Warm temperaturesincrease HFR1 abundance by a combination of increased HFR1 expression and stability (32, 44).The addition of UV-B radiation to the photosynthetic light increases the stability of HFR1 at20°C and 28°C, and, in the presence of UV-B, the hfr1mutant has enhanced hypocotyl growth re-sponse to warm temperature (44). Another atypical bHLH,PACLOBUTRAZOLRESISTANT1(PRE1), interacts with HFR1 (47) and PAR1 (43) to release PIF4 and eventually enhance the re-sponse to warm temperatures, but the dynamics of these components in response to temperatureremains to be characterized.

In PIF4 overexpressors, ELF3 reduces the long-hypocotyl phenotype and the enhanced PIF4-target gene expression, which indicates that ELF3 has an effect that is independent of its role inthe control of PIF4 transcription and the EVENING COMPLEX (76). Like DELLAs, ELF3physically interacts with PIF4 and prevents its binding to its target promoters (76).

The SEUSS (SEU) transcription factor physically interacts with PIF4 and coregulates the ex-pression of many genes (49). SEU appears to enhance the binding of PIF4 to some of its promotersand positively affects hypocotyl growth and gene expression responses to warm temperatures (49),but the effects of temperature on SEU remain to be elucidated.

There are other mechanisms that affect PIF4 binding to DNA. At warm temperatures, PIF4recruits FCA to the chromatin, and, there, FCA induces chromatin modifications that causePIF4 dissociation from its target genes and attenuate the response to the temperature cue (61)(Figure 5). HY5 and PIF4 apparently compete for the same conserved binding sites in YUC8and other target genes potentially involved in growth responses to temperature (38). This is sim-ilar to earlier reports about other PIFs during pigmentation responses to temperature (108).

6.7. Transcriptional Activity of Bound PHYTOCHROME-INTERACTINGFACTOR 4

The transcription factors TIMING OF CAB EXPRESSION1 (TOC1) and PSEUDO-RESPONSE REGULATOR5 (PRR5) are components of the circadian clock and directly in-teract with PIF4 (117). TOC1 closely colocalizes with PIF4 at many gene targets, likely bindingthe same G-box motif, and negatively regulates PIF4 activation of its target gene promoters inprotoplast assays without affecting the binding of PIF4 to these targets (117). Overexpression ofTOC1 or PRR5 results in plants with a reduced response to warmer temperature with respect tohypocotyl growth and PIF4 target gene expression (YUC8, IAA19, and IAA29). However,HSP70(which is not a direct target of PIF4) and PIF4 expression in response to increased temperature andPIF4 stability are unaffected. Conversely, the toc1 mutant shows exaggerated responses to warmtemperatures, and the pif4 mutation is epistatic to this phenotype. TOC1 reduces the ability ofPIF4 to activate its targets (but not the binding of PIF4 to targets) in the evening (when TOC1is expressed), and this confers circadian regulation of temperature cue sensitivity. Conversely, thecircadian regulation of PIF4 expression by ELF3 is at least partially overridden by warm temper-atures because warm temperatures reduce ELF3 binding to the PIF4 promoter (8, 29, 86).

The blue light–activated cryptochrome 1 (cry1) and cry2 photoreceptors also physically in-teract with PIF4 (70, 82), and blue light perceived by cry1 reduces warm temperature–inducedYUC8 expression, auxin accumulation, and hypocotyl growth (70). Blue light has little effect onPIF4 stability (23, 82), but cry1 and PIF4 associate to the same chromatin region in several targetgenes (70).Warm temperature does not significantly affect the abundance of cry1, but it increasesits binding to the PIF4 targets under blue light (70). The presence of cry1 does not affect PIF4


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binding to the YUC8 promoter, but it reduces the ability of PIF4 to enhance YUC8 expression intransient transcription assays (70). PIF4 and BZR1 share a large number of gene targets, but, incontrast to TOC1 and cry1, they synergistically control the expression of these genes (78).

7. HORMONAL REGULATION

7.1. Auxin

Hypocotyl growth and leaf hyponastic responses to warm temperatures are impaired in mutantsdeficient in auxin synthesis, perception, or signaling (39, 104).Warm temperatures increase auxinlevels by stimulating the expression of genes encoding key enzymes in auxin synthesis such asTAA1, CYP79B2, and YUC8. This change in auxin levels results in increased expression of auxin-responsive genes such as Aux/IAAs, GH3s, and SAURs, and the activity of the DR5 syntheticpromoter (33, 39, 104). In young seedlings, expression of the SAUR19, SAUR21, SAUR23, andSAUR24 genes is particularly evident in the hypocotyl, which is the growth-responsive organ (33).

Warm temperatures enhance PIF4 specific binding to the G-box (CACGTG)–containing re-gion of the YUC8 promoter (104) and to the promoter and upstream coding sequences of TAA1and CYP79B2 (33). Since PIF4 was expressed by a constitutive promoter in these experiments,enhanced binding should have resulted from elevated PIF4 protein stability and/or an intrinsi-cally higher DNA-binding capacity of PIF4 under warm temperatures (33). PIF4 also enhancesYUC8 expression in trans-activation assays in Nicotiana benthamiana and TAA1, CYP79B2, YUC8,SAUR19, SAUR24, and DR5 responses are impaired in the pif4 mutant (33, 104). Conversely,in a PIF4 overexpressor line, YUC8 expression and auxin levels are elevated (104). Addition ofa synthetic auxin or overexpression of SAUR19 restores hypocotyl growth in the pif4 mutant atwarm temperature (33), whereas the yuc8 mutation and an iaa19 gain-of-function mutation sig-nificantly reduce the hypocotyl growth promotion induced by PIF4 overexpression (104). Takentogether, these observations indicate that enhanced PIF4 activity under warm temperatures pro-motes hypocotyl growth by elevating auxin levels.

The promotion of YUC8 expression has a peak at 4 h and decreases significantly 8 or 24 hafter the shift to warm temperatures (49, 104). This suggests that beyond early hours, elevatedsensitivity to auxin could have a role as described elsewhere for shade-avoidance responses (84).For instance, warm temperatures rapidly increase the abundance of HSP90, which, together withthe cochaperone SGT1, binds and stabilizes the auxin coreceptor TIR1 (112) and could thereforeincrease the amplitude of the response to a given level of auxin.

SAURproteins induced by auxin inhibit the activity of type-2C protein phosphatases belongingto the D clade (PP2C.D) which in turn inhibit plasma membrane proton-ATPases (101). There-fore, auxin promotes growth by elevating the concentration of protons in the apoplast as the activ-ity of the wall-loosening proteins, expansins, increases at low pH (20). After several hours, warmtemperatures enhance the abundance of selected PP2C.D proteins, apparently by posttranscrip-tional mechanisms, which might prevent exaggerated hypocotyl growth (87).

Although temperature affects primary root growth via auxin (42, 118) and although these ef-fects are deficient in pif4 pif5 (114), the connection between PIF4 and auxin in root growth has notbeen established. In experiments where the seedlings are transferred from 22°C to 16°C or from23°C to 29°C 3–5 days after germination, auxin levels in the root respectively decrease or increasecompared to the controls that remain at 22°C or 23°C (42, 118). In each case, higher auxin levelsenhance root growth largely by increasing meristem size and cell number as a result of a faster rateof cell division (42, 118). Stronger auxin signaling under warmer conditions is particularly obviousat the meristematic zone, whose activity is promoted by auxin. The analysis of expression of genesinvolved in biosynthesis and transport of auxin suggests that both processes would be reduced by


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a shift from 22°C to 16°C (118). The response to temperature requires PIN-FORMED (PIN)auxin efflux carriers and is therefore reduced in the pin1 pin3 pin7 mutant (118). In contrast toroot cell division, root cell elongation is inhibited by auxin. This effect may be counteractedby a more intense shootward-polar movement of auxin under warm temperature mediated bySORTING NEXIN1 (SNX1)–dependent targeting of PIN2 to the plasma membrane ratherthan to the vacuole (42).

7.2. Brassinosteroids

PIF4 enhances the expression of brassinosteroid synthesis genes CONSTITUTIVE PHOTO-MORPHOGENESIS AND DWARFISM (CPD) and DWARF4 (DWF4) in response to warm tem-peratures, particularly late at night (71). The transcription factor BZR1 accumulates in the nu-cleus in warm temperatures, which could be the result of an increase in brassinosteroid synthesis.However, the phosphorylation status of BZR1 (and BZR2), which responds to brassinosteroids,does not appear to respond to temperature (102). BZR1 can subsequently induce PIF4 expression,defining a potential feed-forward loop (51).

There is evidence for a role of brassinosteroid signaling downstream of the PIF4–auxin mod-ule in the control of shoot architecture (51). Exogenously applied brassinosteroids rescue thehypocotyl growth response to warm temperature of the pif4 mutant and of mutants of auxin-synthesis or auxin-perception genes, whereas application of a synthetic auxin does not rescue thetemperature response of mutants impaired in brassinosteroid synthesis or signaling (51). Further-more, addition of an inhibitor of brassinosteroid synthesis eliminates the long-hypocotyl pheno-type caused by PIF4 overexpression. In the primary root, warm temperature reduces the stabil-ity and the abundance of the brassinosteroid receptor BRASSINOSTEROID INSENSITIVE 1(BRI1), and this change could contribute to growth promotion (72).

7.3. Gibberellins

The hypocotyl growth response to temperature is absent in the ga1 mutant impaired in the syn-thesis of gibberellin (102). Furthermore, expression of the gibberellin biosynthesis genesGA20ox1and GA3ox1 is rapidly increased in the hypocotyl after transferring the seedlings to higher tem-peratures. This occurs simultaneously with a marked decrease in the expression of the gibberellin-inactivating enzymeGA2ox1, and some of these genes also respond in the cotyledons (102). Theseobservations suggest a role for increased accumulation of gibberellins in hypocotyls grown inwarm temperatures. In turn, gibberellins affect thermomorphogenesis by inducing reduced sta-bility of DELLA proteins.

8. ECOLOGY OF THERMOMORPHOGENESIS

8.1. Adaptation to Average Temperature

The optimum temperature (80) and theminimum temperature (110) for growth or developmentalprogression tend to be lower for plant species originating from cool areas than for species fromwarm habitats. General responses to temperature show little variability within crop species (80),within A. thaliana accessions (52), and even among species that diverged millions of years ago (80).A slow evolutionary pace may be required to maintain a synchronous shift of different processesand to avoid the loss of coordination of these processes (80). Conversely, specific responses toaverage temperature show intraspecific variability in A. thaliana (52, 91). Several genes harboring


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natural variation, such as ELF3 (8, 86), FLM (68, 69, 105), ICARUS1 (119),CRY2 (91), and PIF4(37), contribute to genetic variability in hypocotyl growth or flowering responses to temperature.

8.2. The Function of Plant Plasticity in Response to Average Temperature

Morphological plasticity in response to average temperature could serve to avoid heat stress (85).Longer hypocotyls could help to move the sensitive apical tissues of the seedling away from thesoil (39), where temperatures are elevated (Figure 1). Leaf hyponasty would reduce the incidenceof midday solar radiation (due to a change in angle between the leaf surface and direct sunlight)and also enhance the ventilation of the leaves (9, 21)—two factors that reduce temperature.

In A. thaliana, warm temperatures reduce the density of stomata (60), which are the poresthrough which leaves release water to the atmosphere. The rate of transpiration is significantlyincreased by higher tissue temperatures, which augment the concentration of water vapor withinthe substomatal cavity and, hence, cause a steeper gradient with the surrounding atmosphere.Lowering stomatal density increases the resistance to water loss and helps to save water. However,since water evaporation inside the substomatal cavity cools down the surrounding tissues, loweringstomatal density can increase rather than decrease the risk of heat damage.

Stronger light tends to reduce the magnitude of thermomorphogenesis. Increasing the fluencerate of red light perceived by phyB (64, 65), blue light perceived by cryptochromes (70), or UV-Bradiation perceived by UVR8 (44), as well as increasing daylength (38), can reduce the impact oftemperature on morphogenesis. The highest risk of heat stress is experienced by plants exposed tofull sunlight under the long days of summer, and yet these are the conditions where the responsesto temperature are reduced. This paradox suggests that rather than avoiding heat stress, theseresponses could serve to enhance shade avoidance; i.e., to maximize hypocotyl growth when aseedling is simultaneously exposed to shade and warm temperatures. The combination of shadeand warm temperatures is risky for survival because low light (shade) restricts the photosyntheticcarbon gain, while high temperatures increase carbon loss through respiration (1).

The induction of flowering by warm spring temperatures may help to adjust the reproductivephase to the favorable season (15), providing another function for thermomorphogenesis. Thisadjustment of developmental timing may of course help to avoid extreme estival temperatures,but, depending on the region, this advantage could be more related to eluding early flowering andthe risk of facing a late frost or to flowering during drought periods.

8.3. Crop and Pasture Yield

Is there thermomorphogenesis in agricultural crops and pastures, or it is just a curiosity ofA. thaliana? A few examples are sufficient to illustrate that temperature changes the final plantor organ morphology in species of economic importance. In soybean (Glycine max), for instance,a 4°C rise in the temperature from 22°C/16°C (day/night) to 26°C/20°C increases stem heightmore than threefold without affecting leaf area (100). In wheat (Triticum aestivum), raising thetemperature from 10°C to 15°C increases the number of leaves (and, hence, the number of budsable to produce tillers or branches) more than the actual number of tillers, and this indicates anenhancement of apical dominance (34). In forage grasses such as tall fescue (Festuca arundinacea),the final length of the leaf lamina can double at temperatures between 10°C and 25°C because theincrease in rate of extension is much larger than the decrease in the duration of growth; laminawidth, however, is largely unaffected within the same range (88). In subterranean clover (Tri-folium subterraneum), specific leaf area (leaf area per unit of leaf weight) is reduced by increasingconstant growth temperature from 15°C to 30°C (36).Differential effects reveal specific responsesto average temperature, i.e., thermomorphogenesis.


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In A. thaliana, warmer temperatures reduce the number of seeds per plant as a result of lowernumbers of both siliques per plant and seeds per silique, although the size of the seeds is largelyunaffected (52). Similarly, in wheat, grain yield decreases gradually between 15°C and 30°C (111).Conversely, in corn (Zea mays), soybean, and cotton (Gossypium sp.), yields increase with temper-ature up to an optimum temperature (these are 29°C, 30°C, and 32°C, respectively) and show asharp decrease beyond that point (94). Of course, these are effects of temperature and not neces-sarily thermomorphogenesis, but it seems unlikely that the significant changes of body shape dueto thermomorphogenesis have no consequences for yield. Interestingly, warm temperature effectson grain yield in Brachypodium have been linked with H2A.Z nucleosomal dynamics (6). A recentanalysis in wheat concluded that knowledge gaps in our understanding of plant responses to tem-perature are a key component of the uncertainty in crop yield projections generated by currentmodels (111). Improving the accuracy of crop productivity estimates is crucial for defining strate-gies that ensure future food security, particularly in a scenario of global climate change (111). Inthis context, a better understanding of thermomorphogenesis in economically-important plantsis urgently needed to generate climate-smart plants.

SUMMARY POINTS

1. Increasing temperature under the optimum value accelerates the pace of plant growthand development, but, in addition to these general effects, selected processes show spe-cific, strong responses that change plant morphology (thermomorphogenesis).

2. Potential functions of thermomorphogenesis include the avoidance of heat stress, exces-sive water loss, or carbon starvation and the adjustment to seasonal change.

3. Key components of the thermomorphogenesis perception–signaling network includechanges in transcription, chromatin remodeling, alternative splicing, phytochrome B(phyB) sensor activity, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) sub-network dynamics, and hormone signaling status.

4. The findings that the phyB photosensory receptor also senses temperature and that sev-eral photomorphogenesis genes (e.g.,PIF4,COP1,HY5), clock genes (e.g.,ELF3,TOC1),and hormone genes (e.g., YUC8, BZR1, DELLAs) are important in thermomorphogen-esis reveal a tight link between light and temperature cues intermingled with temporaland endogenous information in the control of plant morphology.

5. In Arabidopsis thaliana, there is significant genetic variability at key thermomorphogen-esis loci.

6. Thermomorphogenesis is likely to have a significant role in the productivity of cropsand pastures.

FUTURE ISSUES

1. Additional thermosensors and their division of labor remain to be elucidated.

2. Our understanding of the functional links among the components of the thermomor-phogenesis signaling network is limited, and these need to be investigated. Even whenmolecular connections are known, we are largely ignorant of the level of flux throughthese connections.


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3. Exploring the genetic variability and field impact of thermomorphogenesis in organismsbeyond A. thalianawill ensure that plant productivity is responsive to new needs broughtabout by global climate change.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

Research in the laboratory of J.J.C. is funded by the Agencia Nacional de Promoción Científicay Tecnológica, Universidad de Buenos Aires, and the Consejo Nacional de Investigaciones Cien-tíficas y Técnicas (CONICET). Research in the laboratory of S.B. is supported by an AustralianResearch Council Future Fellowship (FT100100377) and the Larkins Fellowship from MonashUniversity.

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Thermomorphogenesis - Universidad de Costa Ricabiologia.ucr.ac.cr/profesores/Garcia...

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