PIFs coordinate shade avoidance by inhibiting auxin repressor ARF18 and metabolic regulator QQS

Abstract

Shade avoidance syndrome (SAS) arises in densely growing plants that compete for light. In Arabidopsis thaliana, phytochrome interacting factor (PIF) proteins link the perception of shade to stem elongation via auxin production. Here, we report that PIFs inhibit the shade-induced expression of AUXIN RESPONSE FACTOR 18 (ARF18), and ARF18 represses auxin signaling. Therefore, PIF-mediated inhibition of ARF18 enhances auxin-dependent hypocotyl elongation in simulated shade. Furthermore, we show that both PIFs and ARF18 directly repress qua-quine starch (QQS), which controls the allocation of carbon and nitrogen. Shade-repressed QQS attenuates the conversion of starch to protein and thus reduced leaf area. Our results suggest that PIF-dependent gene regulation coordinates multiple SAS responses, including altered stem growth via ARF18, as well as altered leaf growth and metabolism via QQS.

Control of Plant Growth and Defense by Photoreceptors: From Mechanisms to Opportunities in Agriculture

“…This is a highly complex network, and this complexity is further increased by the fact that within the ARF family (Roosjen et al, 2017) there are both auxin repressors and activators. A recent study, for example, identified how PIFs inhibit the expression of ARF18, which encodes a transcription factor that inhibits auxin signaling (Jia et al, 2020), whereas other ARFs promote auxin signaling and growth (Reed et al, 2018). Active phyB and cry1 have also been proposed to directly interact with auxin signaling-promoting ARF proteins, such as ARF6 and ARF8, to repress their DNA binding ability (Mao et al, 2020), as well as with specific AUX/IAA proteins where photoreceptor interaction stabilizes AUX/IAAs (Xu et al, 2018).…”

Characterization of Phytochrome-Interacting Factor Genes in Pepper and Functional Analysis of CaPIF8 in Cold and Salt Stress

“…Besides the vital role in photomorphogenesis, PIFs are also involved in the regulation of many other cellular processes, including fruit ripening, flowering time, and hormone response ( Paik et al, 2017 ). For example, Arabidopsis PIFs have important functions in shade avoidance response (SAS) mainly through auxin biosynthesis and auxin signaling ( Hornitschek et al, 2012 ; Hersch et al, 2014 ; Pacín et al, 2016 ; Jia et al, 2020 ), as well as via other phytohormones including gibberellin (GA) and brassinosteroid (BR) ( Feng et al, 2008 ; Sorin et al, 2009 ; Xie et al, 2017 ; Hayes et al, 2019 ; Wang X. et al, 2020 ). Additionally, PIF1, PIF3, PIF4, PIF5, and PIF7 are necessary for the phy-mediated seasonal regulation of hypocotyl elongation in Arabidopsis ( Leivar et al, 2020 ).…”

Light participates in the auxin‐dependent regulation of plant growth

“…Photoreceptors directly interact with essential component factors involved in auxin signaling transduction pathway, and two recent studies point out that light can also regulate AUX/IAAs or ARFs by PIFs (Pucciariello et al, 2018; Jia et al, 2020) (Figure 1). Pucciariello et al, (2018) found that prolonged shade‐maintained elevated levels of PIF4 in the hypocotyl directly activate the expression of IAA19 and IAA29 , which in turn reduce the expression of the growth‐repressive IAA17 and abundance of ARF6 to sustain shade avoidance.…”

“…Pucciariello et al, (2018) found that prolonged shade‐maintained elevated levels of PIF4 in the hypocotyl directly activate the expression of IAA19 and IAA29 , which in turn reduce the expression of the growth‐repressive IAA17 and abundance of ARF6 to sustain shade avoidance. Jia et al, (2020) showed that PIFs attenuated the shade‐induced up‐regulation of AFR18 , an auxin signaling repressor, to enhance auxin‐dependent hypocotyl elongation in simulated shade.…”

“…PIF4 has dual roles in regulating downstream target genes. It can up‐regulate the expression of YUCs (Hornitschek et al, 2012) and IAA19/29 (Pucciariello et al, 2018), while down‐regulating the expression of UGT76F1 (Chen et al, 2020) and ARF18 (Jia et al, 2020) to enhance the auxin biosynthesis and signaling eventually (Figure 1). It is unclear how PIF4 identifies downstream factors and regulates them differently to achieve the same effect.…”