Take it easy in the heat: Transcription factors PIF4 and TCP4 interplay to slow leaf growth

Plants face a variety of high-temperature episodes that substantially impact their yield and productivity, but how do plants survive such unfavorable climatic conditions? Compensatory adaptive mechanisms, such as stomatal closure, hypocotyl elongation, and early flowering, allow plants to thrive in high temperatures (Mishra et al., 2021) and have been extensively studied (Koini et al., 2009; Quint et al., 2016; Kim et al., 2020).

Changes in leaf orientation also affect survival under high temperature. Kim et al. (2020) have shown that the leaf is highly sensitive to high temperature and provides cues for thermoresponsive growth to other aerial tissues (Kim et al., 2020). Previous investigations have provided mechanistic insights into changes in leaf architectural attributes, notably shape and petiole angle under high temperature (Nakayama et al., 2014; Sicard et al., 2014; Ibañez et al., 2017); however, the underlying mechanism of high temperature-mediated alterations of leaf size is still largely unexplored.

In the present issue of Plant Physiology, Saini et al. (2022) studied the mechanism of high-temperature mediated alterations in leaf plasticity. The authors measured Arabidopsis (Arabidopsis thaliana) leaf morphological and cellular attributes, notably leaf area and epidermal and palisade cell numbers of rosette leaves The results suggested that leaf area and cell number are reduced under high-temperature exposure. The authors hypothesized that the reduced cell number might be due to impaired cell division and validated their hypothesis using cell cycle marker, cell cycle progression marker, and DAPI staining to show that cell division is restricted in high temperatures.

PHYTOCHROME INTERACTING FACTOR 4 (PIF4) is a major determinant of plant architecture under high temperatures (Quint et al., 2016), and high temperature-induced PIF4 accumulation directs auxin movement to the abaxial side of the petiole to lower leaf temperature (Park et al., 2019). Leaf epidermis-specific PIF4 induces the constitutive hypocotyl elongation under high temperatures (Kim et al., 2020).

Therefore, Saini et al. explored the role of PIF4 in leaf growth under high temperatures using a PIF4 promoter GUS line and translational reporter line. PIF4 was translationally more active under high temperature than under control conditions. The pif4 mutant showed no change in rosette leaf area, number of palisade cells, pavement cell number, and leaf phenotype under high temperature as compared to the control. Therefore, the authors concluded that PIF4 can control leaf size determination in coordination with cell division. Further, they examined the high temperature-induced transcriptome in leaves and identified other genetic determinants involved in heat responses, such as several members of the TEOSINTE BRANCHED1/CYCLOIDEA/PCFs (TCP) transcription factor (TF) family. The tcp4 mutant showed no difference in leaf area and minimal reduction in cell number compared to the Col-0 wild type under high temperature, indicating that TCP4 might also participate in high temperature mediated alteration in cell division.

Since the mutant lines of PIF4 and TCP4 showed the same phenotype under high temperature, the authors hypothesized that both TFs might participate in a common pathway to control leaf size. pif4 tcp4 double mutant lines showed no change in leaf area and cell number under high temperature. A previous study showed that TCP4 binds to the promoter region of KIP-RELATED PROTEIN1 (KRP1, a cell cycle inhibitor) and possibly contributes to the inhibition of cell division (Schommer et al., 2014). However, the authors found KRP1 expression in the double mutant was reduced by comparison with either of the single mutants, suggesting that both PIF4 and TCP4 function together to control KRP1 expression.

Intriguingly, although the binding of TCP4/PIF4 to the KRP1 promoter increased with temperature, the authors could not identify any binding of PIF4 in the tcp4 mutant. Further coimmunoprecipitation showed increased enrichment in two putative TCP4 binding sites in the PIF4 promoter under high temperature. These findings suggested that binding of PIF4 to the KRP1 promoter is TCP4 dependent. The present study revealed a function of PIF4 and its collaboration with the developmental regulator TCP4 in controlling leaf size under high temperatures (Figure 1). This mechanism provides insight into the morphological adaption of plant fitness in a non-ambient environment. However, the targets of the PIF4 and TCP4 nexus have not been explored. Hence, a detailed investigation of targets would provide a better understanding of the high temperature-mediated leaf size mechanism that helps fine-tune leaf size and increases plant fitness.

Figure 1.

Schematic of high-temperature mediated leaf suppression. High temperature activates TFs PIF4 and TCP4, which induce cell cycle inhibitor KRP1 expression, which in turn suppresses the cell cycle.

Conflict of interest statement. There is no conflict of interest.