Functions of Phytochrome Interacting Factors (PIFs) in Adapting Plants to Biotic and Abiotic Stresses

Abstract

Plants possess the remarkable ability to sense detrimental environmental stimuli and launch sophisticated signal cascades that culminate in tailored responses to facilitate their survival, and transcription factors (TFs) are closely involved in these processes. Phytochrome interacting factors (PIFs) are among these TFs and belong to the basic helix-loop-helix family. PIFs are initially identified and have now been well established as core regulators of phytochrome-associated pathways in response to the light signal in plants. However, a growing body of evidence has unraveled that PIFs also play a crucial role in adapting plants to various biological and environmental pressures. In this review, we summarize and highlight that PIFs function as a signal hub that integrates multiple environmental cues, including abiotic (i.e., drought, temperature, and salinity) and biotic stresses to optimize plant growth and development. PIFs not only function as transcription factors to reprogram the expression of related genes, but also interact with various factors to adapt plants to harsh environments. This review will contribute to understanding the multifaceted functions of PIFs in response to different stress conditions, which will shed light on efforts to further dissect the novel functions of PIFs, especially in adaption to detrimental environments for a better survival of plants.

Keywords: abiotic stresses; biotic stress; phytochrome interacting factors.

Figure 1

Bioinformatics analysis of PIFs proteins. (A) The phylogenetic evolutionary tree of PIF proteins, constructed using MEGA-X, was divided into five groups (Groups I–V), and was further esthetically enhanced using Evolview. (B) The PIF proteins were subjected to multiple sequence alignment using DNAMAN, and the characteristic structural domains, namely APB, APA, and bHLH, were marked. Different colors are used to indicate the similarity of multiple sequence alignments. (Black = 100%, pink > 75%, blue > 50%, yellow > 30%) (C) Motif analysis on PIF proteins used MEME, and the 12 analyzed motifs are visualized on the right. Chiclop is used to beautify the images. The protein sequences used for analysis are TaPIF1-1A (TraesCS1A02G083000.1), TaPIF1-1B (TraesCS1B02G100400.1), TaPIF1-1D (TraesCS1D02G084200.1), TaPIF2-1A (TraesCS1A02G212700.1), TaPIF2-1B (TraesCS1B02G226200.1), TaPIF2-1D (TraesCS1D02G215600.1), TaPIF3-2A (TraesCS2A02G253900.1), TaPIF3-2B (TraesCS2B02G273500.1), TaPIF3-2D (TraesCS2D02G254400.1), TaPIF4-5A (TraesCS5A02G049600.1), TaPIF4-5B (TraesCS5B02G054800.1), TaPIF4-5C (TraesCS5D02G060300.1), TaPIF5-5A (TraesCS5A02G376500.1), TaPIF5-5B (TraesCS5B02G380200.1), TaPIF5-5D (TraesCS5D02G386500.1), TaPIF6-5A (TraesCS5A02G420200.1), TaPIF6-5B (TraesCS5B02G422000.1), PtPIF1 (Potri.002G252800.9), PtPIF3a (Potri.005G001800.1), PtPIF3b (Potri.013G001300.4), PtPIF4/5a (Potri.002G055400.11), PtPIF4/5b (Potri.005G207200.12), PtPIF8a (Potri.002G143300.1), PtPIF8b (Potri.014G066500.1), PtPIF9a (Potri.005G139700.2), PtPIF9b (Potri.014G025800.1), PtPIF10 (Potri.014G111400.1), CmPIF1 (MELO3C012808.2), CmPIF3 (MELO3C031303.2), CmPIF4 (MELO3C026410.2), CmPIF8 (MELO3C022233.2), GhPIF1-1a (Gh_A11G1248.1), GhPIF1-1d (Gh_D11G1395), GhPIF1-2d (Gh_D07G1543), GhPIF1-3d (Gh_D05G3213), GhPIF1-4d (Gh_D07G2050.1), GhPIF2a (Gh_A11G3067), GhPIF2d (Gh_D11G1107), GhPIF3a (Gh_A11G2494), GhPIF3d (Gh_D11G2839), GhPIF6a (Gh_A07G1202), GhPIF6d (Gh_D07G1303), GhPIF7-1 (Gh_A03G0607), GhPIF7-1d (Gh_D03G0895), GhPIF7-2d (Gh_D07G0698), GhPIF8a (Gh_A11G0710), GhPIF8d (Gh_D11G0826), GhPIF9-1a (Gh_A07G0148), GhPIF9-1d (Gh_D07G0141), GhPIF9-2d (Gh_D09G2368), GhPIF9-3d (Gh_D11G1337), GhPIF9-4a (Gh_A08G1091), GhPIF9-4d (Gh_D08G1374), GhPIF9-5a (Gh_A10G1164), GhPIF9-5d (Gh_D10G1331), AtPIF1 (AT2G20180.2), AtPIF3 (AT1G09530.1), AtPIF4 (AT2G43010.5), AtPIF5 (AT3G59060.2), AtPIF6 (AT3G62090.2), AtPIF7 (AT5G61270.1), OsPIL11 (Os12g0610200), OsPIL12 (Os03g0639300), OsPIL13 (Os03g0782500), OsPIL14 (Os07g0143200), OsPIL15 (Os01g0286100), OsPIL16 (Os05g0139100), ZmPIF1 (GRMZM2G115960_P03), ZmPIF3 (Zm00001eb332400_P001), ZmPIF5.2 (Zm00001eb213550_P001), ZmPIF5.1 (Zm00001eb059460_P001), ZmPIF4.2/5 (Zm00001eb050790_P001), ZmPIF4/4.1 (Zm00001eb031560_P001), ZmPIF3.3 (Zm00001eb417610_P001), SlPIF1a (XP_004247109.1), SlPIF1b (XP_004240467.1), SlPIF3 (XP_010313958.1), SlPIF4/5 (XP_004243631.1), SlPIF7 (XP_004242180.1), SlPIF8 (XP_004229781.1), MdPIF1 (MD10G1170600), MdPIF2 (MD04G1185100), MdPIF3 (LOC103450807), MdPIF4 (MD17G1132600), MdPIF5 (MD09G1146000), MdPIF7 (MD14G1208000), MdPIF8 (MD07G1113200).

Figure 2

A typical molecular model demonstrates how PIFs regulate adaptability to abiotic stress. PIFs, responsive to abiotic stress, can be induced to express or undergo phosphorylation by other protein kinases, thus perceiving abiotic stress signals. Following this, PIFs convey these signals downstream, initiating a multitude of signaling cascades. A symphony of secondary signals and plant hormones collaboratively fine-tune a sophisticated molecular mechanism, triggering a comprehensive array of regulatory elements. This orchestrates the holistic transcriptional reprogramming of a diverse range of genes associated with abiotic stress. In the model diagram, red rounded rectangles represent different PIF proteins, light green rounded rectangles represent different PIF interacting proteins, and the blue rounded rectangles indicate target genes directly regulated by PIFs. Symbols: ˧ indicates negative regulation; → indicates positive regulation. Abbreviations: OsDREB1B, oryza sativa dehydration responsive element binding; COR, cold-responsive gene; CBF, C-repeat binding factors; GAI4, gibberellic acid insensitive 4; SlTDF, tapetal development and function 1; SlDYT, dysfunctional tapetum 1; SPAs, suppressor of phyA-105; TCP4, teosinte branched1/cycloidea/pcf4; KPR1, KIP-related protein 1; HSFA2, heat shock factor A2; ORE1, oresara1; IAA29, indole-3-acetic acid inducible 29; SPCH, SPEECHLESS; SOS2, salt overly sensitive 2; JUB1, jungbrunnen 1; SAG29, senescence-associated gene 29; OsSLR1, slender rice 1; EXP4, expansin 4.

Figure 3

A schematic model illustrates how PIFs counteract biotic stress through various pathways. PIFs play a crucial role in plant immunity by directly regulating downstream defense-related genes and participating in the signal transduction of classic defense pathways, such as JA/ETH and SA, thereby orchestrating the plant’s immune response. In the model diagram, red rounded rectangles represent different PIF proteins; light green rounded rectangles represent different PIF interacting proteins; and blue rounded rectangles indicate target genes directly regulated by PIF binding. Symbols: ˧ indicates negative regulation; → indicates positive regulation. Abbreviations: MAPK, mitogen-activated protein kinases; IOS1, iron-deficiency overly sensitive; JAZ, jasmonate ZIM-domain; COI, coronatine insensitive 1; ERF, ethylene responsive factor; ST2A, sulfotransferase; MYC, myelocytomatosis; ICS, isochorismate synthate; RDR6, RNA-dependent RNA polymerase 6; AGO1, argonaute 1.