Interaction of Shade Avoidance and Auxin Responses: a Role for Two Novel Atypical BHLH Proteins

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2007 Oct 20

PMID 17948056

Citations 110

Authors

Irma Roig-Villanova

Jordi Bou-Torrent

Anahit Galstyan

Lorenzo Carretero-Paulet

Sergi Portoles

Manuel Rodriguez-Concepcion

Jaime F Martinez-Garcia

Affiliations

Soon will be listed here.

Abstract

Plants sense the presence of potentially competing nearby individuals as a reduction in the red to far-red ratio of the incoming light. In anticipation of eventual shading, a set of plant responses known as the shade avoidance syndrome (SAS) is initiated soon after detection of this signal by the phytochrome photoreceptors. Here we analyze the function of PHYTOCHROME RAPIDLY REGULATED1 (PAR1) and PAR2, two Arabidopsis thaliana genes rapidly upregulated after simulated shade perception. These genes encode two closely related atypical basic helix-loop-helix proteins with no previously assigned function in plant development. Using reverse genetic approaches, we show that PAR1 and PAR2 act in the nucleus to broadly control plant development, acting as negative regulators of a variety of SAS responses, including seedling elongation and photosynthetic pigment accumulation. Molecularly, PAR1 and PAR2 act as direct transcriptional repressors of two auxin-responsive genes, SMALL AUXIN UPREGULATED15 (SAUR15) and SAUR68. Additional results support that PAR1 and PAR2 function in integrating shade and hormone transcriptional networks, rapidly connecting phytochrome-sensed light changes with auxin responsiveness.

Citing Articles

Genome-wide identification and expression analysis of () genes in rice ().

Jia C, Shi Y, Wang H, Zhang Y, Luo F, Li Z Plant Signal Behav. 2024; 19(1):2391658.

PMID: 39148317 PMC: 11328882. DOI: 10.1080/15592324.2024.2391658.

Temporal and spatial frameworks supporting plant responses to vegetation proximity.

Pastor-Andreu P, Moreno-Romero J, Urdin-Bravo M, Palau-Rodriguez J, Paulisic S, Kastanaki E Plant Physiol. 2024; 196(3):2048-2063.

PMID: 39140970 PMC: 11531833. DOI: 10.1093/plphys/kiae417.

Natural variation in response to combined water and nitrogen deficiencies in Arabidopsis.

Xue Z, Ferrand M, Gilbault E, Zurfluh O, Clement G, Marmagne A Plant Cell. 2024; 36(9):3378-3398.

PMID: 38916908 PMC: 11371182. DOI: 10.1093/plcell/koae173.

Genome-wide characterization of the bHLH gene family in Gynostemma pentaphyllum reveals its potential role in the regulation of gypenoside biosynthesis.

Qin Y, Li J, Chen J, Yao S, Li L, Huang R BMC Plant Biol. 2024; 24(1):205.

PMID: 38509465 PMC: 10953245. DOI: 10.1186/s12870-024-04879-y.

Capture of regulatory factors via CRISPR-dCas9 for mechanistic analysis of fine-tuned SERRATE expression in Arabidopsis.

Chen W, Wang J, Wang Z, Zhu T, Zheng Y, Hawar A Nat Plants. 2024; 10(1):86-99.

PMID: 38168608 DOI: 10.1038/s41477-023-01575-x.

References

Nemhauser J, Mockler T, Chory J . Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2004; 2(9):E258. PMC: 509407. DOI: 10.1371/journal.pbio.0020258. View

Buck M, Atchley W . Phylogenetic analysis of plant basic helix-loop-helix proteins. J Mol Evol. 2003; 56(6):742-50. DOI: 10.1007/s00239-002-2449-3. View

Martinez-Garcia J, Huq E, Quail P . Direct targeting of light signals to a promoter element-bound transcription factor. Science. 2000; 288(5467):859-63. DOI: 10.1126/science.288.5467.859. View

Ni M, Tepperman J, Quail P . PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell. 1998; 95(5):657-67. DOI: 10.1016/s0092-8674(00)81636-0. View

Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T . Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development. 1999; 126(19):4235-45. DOI: 10.1242/dev.126.19.4235. View

Khanna R, Shen Y, Toledo-Ortiz G, Kikis E, Johannesson H, Hwang Y . Functional profiling reveals that only a small number of phytochrome-regulated early-response genes in Arabidopsis are necessary for optimal deetiolation. Plant Cell. 2006; 18(9):2157-71. PMC: 1560915. DOI: 10.1105/tpc.106.042200. View

Devlin P, Robson P, Patel S, Goosey L, Sharrock R, Whitelam G . Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiol. 1999; 119(3):909-15. PMC: 32105. DOI: 10.1104/pp.119.3.909. View

Yang J, Lin R, Sullivan J, Hoecker U, Liu B, Xu L . Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell. 2005; 17(3):804-21. PMC: 1069700. DOI: 10.1105/tpc.104.030205. View

Hensel L, Nelson M, Richmond T, Bleecker A . The fate of inflorescence meristems is controlled by developing fruits in Arabidopsis. Plant Physiol. 1994; 106(3):863-76. PMC: 159609. DOI: 10.1104/pp.106.3.863. View

10.

Huq E, Al-Sady B, Hudson M, Kim C, Apel K, Quail P . Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science. 2004; 305(5692):1937-41. DOI: 10.1126/science.1099728. View

11.

Ferre-DAmare A, Prendergast G, Ziff E, Burley S . Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature. 1993; 363(6424):38-45. DOI: 10.1038/363038a0. View

12.

Page R . TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996; 12(4):357-8. DOI: 10.1093/bioinformatics/12.4.357. View

13.

Quail P . Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol. 2002; 3(2):85-93. DOI: 10.1038/nrm728. View

14.

Chen M, Chory J, Fankhauser C . Light signal transduction in higher plants. Annu Rev Genet. 2004; 38:87-117. DOI: 10.1146/annurev.genet.38.072902.092259. View

15.

Martinez-Garcia J, Virgos-Soler A, Prat S . Control of photoperiod-regulated tuberization in potato by the Arabidopsis flowering-time gene CONSTANS. Proc Natl Acad Sci U S A. 2002; 99(23):15211-6. PMC: 137569. DOI: 10.1073/pnas.222390599. View

16.

Wray G, Hahn M, Abouheif E, Balhoff J, Pizer M, Rockman M . The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol. 2003; 20(9):1377-419. DOI: 10.1093/molbev/msg140. View

17.

Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J . A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell. 2005; 120(2):249-59. DOI: 10.1016/j.cell.2004.11.044. View

18.

Alonso J, Stepanova A, Leisse T, Kim C, Chen H, Shinn P . Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003; 301(5633):653-7. DOI: 10.1126/science.1086391. View

19.

Huq E, Quail P . PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 2002; 21(10):2441-50. PMC: 126004. DOI: 10.1093/emboj/21.10.2441. View

20.

Atchley W, FITCH W . A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A. 1997; 94(10):5172-6. PMC: 24651. DOI: 10.1073/pnas.94.10.5172. View