PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature

Abstract

At high ambient temperature, plants display dramatic stem elongation in an adaptive response to heat. This response is mediated by elevated levels of the phytohormone auxin and requires auxin biosynthesis, signaling, and transport pathways. The mechanisms by which higher temperature results in greater auxin accumulation are unknown, however. A basic helix-loop-helix transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), is also required for hypocotyl elongation in response to high temperature. PIF4 also acts redundantly with its homolog, PIF5, to regulate diurnal growth rhythms and elongation responses to the threat of vegetative shade. PIF4 activity is reportedly limited in part by binding to both the basic helix-loop-helix protein LONG HYPO-COTYL IN FAR RED 1 and the DELLA family of growth-repressing proteins. Despite the importance of PIF4 in integrating multiple environmental signals, the mechanisms by which PIF4 controls growth are unknown. Here we demonstrate that PIF4 regulates levels of auxin and the expression of key auxin biosynthesis genes at high temperature. We also identify a family of SMALL AUXIN UP RNA (SAUR) genes that are expressed at high temperature in a PIF4-dependent manner and promote elongation growth. Taken together, our results demonstrate direct molecular links among PIF4, auxin, and elongation growth at high temperature.indole-3-acetic acid | TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 | CYP79B2 T he hormone indole-3-acetic acid (IAA, or auxin) is fundamental to plant growth and development, controlling many key aspects of shoot and root growth (1). When plants are grown at elevated temperatures, IAA levels increase, resulting in increased hypocotyl elongation (2, 3). Although genetic studies in Arabidopsis have demonstrated that this growth response is dependent on auxin biosynthesis, signaling, and transport pathways, precisely how high temperature promotes an increase in auxin levels has not been established. There are multiple pathways for the de novo synthesis of IAA, the major naturally occurring plant auxin, which are often classified according to whether or not they require the precursor tryptophan (4). Although progress has been made in elucidating some of the enzymes involved in IAA biosynthesis, our understanding of these pathways and their regulation remains rudimentary.In addition to auxin, the basic helix-loop-helix transcription factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) is also required for temperature-dependent hypocotyl elongation (5, 6). PIF4 has emerged as a key regulator of elongation in response to external signals, such as temperature and light, as well as internal signals, including gibberellin and the circadian clock (7-12). In the present work, we investigated potential mechanistic links between PIF4 and IAA in the control of temperatureinduced hypocotyl elongation. We found that PIF4 promotes IAA biosynthesis, possibly by activating the expression of key IAA biosynthetic genes in a temperature-dependent manner. Results and DiscussionGiven that s...

PIFs: Systems Integrators in Plant Development

“…PIFs might also directly repress the JA-regulated transcriptional repressor JAZ9 (Supplemental Table 1), which suggests a regulatory loop between JAs and PIFs ( Figure 5A). The relevance of the regulation of these genes by the PIFs is illustrated by SAUR19 and PRE1, which rescue the short hypocotyl phenotype of pif4 mutants in high temperature and of pifq mutants in Rc, respectively, when overexpressed (Franklin et al, 2011;Oh et al, 2012). In addition, genome-wide transcriptional analyses and binding site identification are uncovering potential PIF targets that are hormone-related genes with a described role in various aspects of photomorphogenesis, but as yet uncharacterized with respect to their function as components in PIF signaling (Supplemental Table 1; Figure 5B).…”

“…In turn, PIFs are also proposed to regulate auxin signaling by inducing the expression of several AUX/IAA and SAUR genes during deetiolation, shade, diurnal growth, and high-temperature responses (Franklin et al, 2011;Nozue et al, 2011;Hornitschek et al, 2012;Leivar et al, 2012b;Li et al, 2012). Interestingly, IAA19 and IAA29 (Sun et al, 2013), as well as SAUR19 (Franklin et al, 2011), are shown to participate in phototropic and high-temperature responses, respectively, downstream of the PIFs. During hook formation, PIFs regulate auxin transport by directly inducing WAG2 (Willige et al, 2012) and ethylene levels by directly inducing ACS5 and ACS8 expression Gallego-Bartolomé et al, 2011).…”

“…Several PIFs induce de novo synthesis of auxin by directly inducing the expression of auxin biosynthetic genes, including YUCCA8 and YUCCA9 in response to shade (Hornitschek et al, 2012;Li et al, 2012), YUCCA8, TAA1, and CYP79B2 in response to high temperature (Franklin et al, 2011;Sun et al, 2012), and possibly YUCCA8 during growth in diurnal conditions (Nozue et al, 2011). In turn, PIFs are also proposed to regulate auxin signaling by inducing the expression of several AUX/IAA and SAUR genes during deetiolation, shade, diurnal growth, and high-temperature responses (Franklin et al, 2011;Nozue et al, 2011;Hornitschek et al, 2012;Leivar et al, 2012b;Li et al, 2012). Interestingly, IAA19 and IAA29 (Sun et al, 2013), as well as SAUR19 (Franklin et al, 2011), are shown to participate in phototropic and high-temperature responses, respectively, downstream of the PIFs.…”

Phytochromes and Phytochrome Interacting Factors

“…Among all known PIFs, PIF4 uniquely regulates hypocotyl elongation in response to light, shade, temperature, and diurnal conditions Lorrain et al, 2008;Franklin et al, 2011;Kumar et al, 2012). It does so by binding to the promoter sequences and activating the expression of target genes, including regulatory genes involved in auxin biosynthesis.…”

Impact of plant shoot architecture on leaf cooling: a coupled heat and mass transfer model

“…Architectural responses to growth at elevated temperatures include elongation of stems and petioles (leaf stems), and increased leaf angles from the soil surface (hyponasty), as observed in the model species Arabidopsis thaliana (figure 1). The promotion of elongation growth at high temperature involves elevation of the plant hormone auxin, and the molecular control of this process is starting to be elucidated [1,[3][4][5]. Despite the striking nature of these phenotypes, their potential physiological significance remains speculative.…”