KAI2 Regulates Seedling Development by Mediating Light-induced Remodelling of Auxin Transport

Overview

Journal New Phytol

Specialty Biology

Date 2022 Mar 21

PMID 35313031

Authors

Maxime Hamon-Josse

Jose Antonio Villaecija-Aguilar

Karin Ljung

Ottoline Leyser

Caroline Gutjahr

Tom Bennett

Affiliations

Soon will be listed here.

Abstract

Photomorphogenic remodelling of seedling growth is a key developmental transition in the plant life cycle. The α/β-hydrolase signalling protein KARRIKIN-INSENSITIVE2 (KAI2), a close homologue of the strigolactone receptor DWARF14 (D14), is involved in this process, but it is unclear how the effects of KAI2 on development are mediated. Here, using a combination of physiological, pharmacological, genetic and imaging approaches in Arabidopsis thaliana (Heynh.) we show that kai2 phenotypes arise because of a failure to downregulate auxin transport from the seedling shoot apex towards the root system, rather than a failure to respond to light per se. We demonstrate that KAI2 controls the light-induced remodelling of the PIN-mediated auxin transport system in seedlings, promoting a reduction in PIN7 abundance in older tissues, and an increase of PIN1/PIN2 abundance in the root meristem. We show that removing PIN3, PIN4 and PIN7 from kai2 mutants, or pharmacological inhibition of auxin transport and synthesis, is sufficient to suppress most kai2 seedling phenotypes. We conclude that KAI2 regulates seedling morphogenesis by its effects on the auxin transport system. We propose that KAI2 is not required for the light-mediated changes in PIN gene expression but is required for the appropriate changes in PIN protein abundance within cells.

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References

Zhao H, Bao Y . PIF4: Integrator of light and temperature cues in plant growth. Plant Sci. 2021; 313:111086. DOI: 10.1016/j.plantsci.2021.111086. View

Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O . The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol. 2006; 16(6):553-63. DOI: 10.1016/j.cub.2006.01.058. View

Lee I, Choi S, Lee S, Soh M . KAI2-KL signaling intersects with light-signaling for photomorphogenesis. Plant Signal Behav. 2019; 14(4):e1588660. PMC: 6512941. DOI: 10.1080/15592324.2019.1588660. View

Wang L, Xu Q, Yu H, Ma H, Li X, Yang J . Strigolactone and Karrikin Signaling Pathways Elicit Ubiquitination and Proteolysis of SMXL2 to Regulate Hypocotyl Elongation in Arabidopsis. Plant Cell. 2020; 32(7):2251-2270. PMC: 7346549. DOI: 10.1105/tpc.20.00140. View

Wang L, Wang B, Jiang L, Liu X, Li X, Lu Z . Strigolactone Signaling in Arabidopsis Regulates Shoot Development by Targeting D53-Like SMXL Repressor Proteins for Ubiquitination and Degradation. Plant Cell. 2015; 27(11):3128-42. PMC: 4682305. DOI: 10.1105/tpc.15.00605. View

Machin D, Hamon-Josse M, Bennett T . Fellowship of the rings: a saga of strigolactones and other small signals. New Phytol. 2019; 225(2):621-636. DOI: 10.1111/nph.16135. View

Shinohara N, Taylor C, Leyser O . Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 2013; 11(1):e1001474. PMC: 3558495. DOI: 10.1371/journal.pbio.1001474. View

Stanga J, Morffy N, Nelson D . Functional redundancy in the control of seedling growth by the karrikin signaling pathway. Planta. 2016; 243(6):1397-406. PMC: 7676495. DOI: 10.1007/s00425-015-2458-2. View

Bennett T, Hines G, van Rongen M, Waldie T, Sawchuk M, Scarpella E . Connective Auxin Transport in the Shoot Facilitates Communication between Shoot Apices. PLoS Biol. 2016; 14(4):e1002446. PMC: 4847802. DOI: 10.1371/journal.pbio.1002446. View

10.

Soundappan I, Bennett T, Morffy N, Liang Y, Stanga J, Abbas A . SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis. Plant Cell. 2015; 27(11):3143-59. PMC: 4682302. DOI: 10.1105/tpc.15.00562. View

11.

Khosla A, Morffy N, Li Q, Faure L, Chang S, Yao J . Structure-Function Analysis of SMAX1 Reveals Domains That Mediate Its Karrikin-Induced Proteolysis and Interaction with the Receptor KAI2. Plant Cell. 2020; 32(8):2639-2659. PMC: 7401016. DOI: 10.1105/tpc.19.00752. View

12.

Xu J, Scheres B . Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell. 2005; 17(2):525-36. PMC: 548823. DOI: 10.1105/tpc.104.028449. View

13.

Waters M, Scaffidi A, Moulin S, Sun Y, Flematti G, Smith S . A Selaginella moellendorffii Ortholog of KARRIKIN INSENSITIVE2 Functions in Arabidopsis Development but Cannot Mediate Responses to Karrikins or Strigolactones. Plant Cell. 2015; 27(7):1925-44. PMC: 4531350. DOI: 10.1105/tpc.15.00146. View

14.

Franklin K, Whitelam G . Light signals, phytochromes and cross-talk with other environmental cues. J Exp Bot. 2003; 55(395):271-6. DOI: 10.1093/jxb/erh026. View

15.

Wang L, Wang B, Yu H, Guo H, Lin T, Kou L . Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature. 2020; 583(7815):277-281. DOI: 10.1038/s41586-020-2382-x. View

16.

Carbonnel S, Das D, Varshney K, Kolodziej M, Villaecija-Aguilar J, Gutjahr C . The karrikin signaling regulator SMAX1 controls root and root hair development by suppressing ethylene biosynthesis. Proc Natl Acad Sci U S A. 2020; 117(35):21757-21765. PMC: 7474694. DOI: 10.1073/pnas.2006111117. View

17.

Lavenus J, Goh T, Roberts I, Guyomarch S, Lucas M, De Smet I . Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 2013; 18(8):450-8. DOI: 10.1016/j.tplants.2013.04.006. View

18.

Sun Y, Flematti G, Smith S, Waters M . Reporter Gene-Facilitated Detection of Compounds in Leaf Extracts that Activate the Karrikin Signaling Pathway. Front Plant Sci. 2016; 7:1799. PMC: 5133242. DOI: 10.3389/fpls.2016.01799. View

19.

Waters M, Smith S . KAI2- and MAX2-mediated responses to karrikins and strigolactones are largely independent of HY5 in Arabidopsis seedlings. Mol Plant. 2012; 6(1):63-75. DOI: 10.1093/mp/sss127. View

20.

Scaffidi A, Waters M, Sun Y, Skelton B, Dixon K, Ghisalberti E . Strigolactone Hormones and Their Stereoisomers Signal through Two Related Receptor Proteins to Induce Different Physiological Responses in Arabidopsis. Plant Physiol. 2014; 165(3):1221-1232. PMC: 4081333. DOI: 10.1104/pp.114.240036. View