Abstract
Main conclusion
SMAX1 and SMXL2 control seedling growth, demonstrating functional redundancy within a gene family that mediates karrikin and strigolactone responses.
Strigolactones (SLs) are plant hormones with butenolide moieties that control diverse aspects of plant growth, including shoot branching. Karrikins (KARs) are butenolide molecules found in smoke that enhance seed germination and seedling photomorphogenesis. In Arabidopsis thaliana, SLs and KARs signal through the α/β hydrolases D14 and KAI2, respectively. The F-box protein MAX2 is essential for both signaling pathways. SUPPRESSOR OF MAX2 1 (SMAX1) plays a prominent role in KAR-regulated growth downstream of MAX2, and SMAX1-LIKE genes SMXL6, SMXL7, and SMXL8 mediate SL responses. We previously found that smax1 loss-of-function mutants display constitutive KAR response phenotypes, including reduced seed dormancy and hypersensitive growth responses to light in seedlings. However, smax1 seedlings remain slightly responsive to KARs, suggesting that there is functional redundancy in karrikin signaling. SMXL2 is a strong candidate for this redundancy because it is the closest paralog of SMAX1, and because its expression is regulated by KAR signaling. Here, we present evidence that SMXL2 controls hypocotyl growth and expression of the KAR/SL transcriptional markers KUF1, IAA1, and DLK2 redundantly with SMAX1. Hypocotyl growth in the smax1 smxl2 double mutant is insensitive to KAR and SL, and etiolated smax1 smxl2 seedlings have reduced hypocotyl elongation. However, smxl2 has little or no effect on seed germination, leaf shape, or petiole orientation, which appear to be predominantly controlled by SMAX1. Neither SMAX1 nor SMXL2 affect axillary branching or inflorescence height, traits that are under SL control. These data support the model that karrikin and strigolactone responses are mediated by distinct subclades of the SMXL family, and further the case for parallel butenolide signaling pathways that evolved through ancient KAI2 and SMXL duplications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- KAR:
-
Karrikin
- SL:
-
Strigolactone
- KL:
-
KAI2 ligand
- SMAX1 :
-
SUPPRESSOR OF MAX2 1
- SMXL :
-
SMAX1-LIKE
- D3 (14, 53) :
-
DWARF3 (14, 53)
- PIN1 :
-
PIN-FORMED1
- KAI2 :
-
KARRIKIN INSENSITIVE2
- MAX2 :
-
MORE AXILLARY GROWTH2
- DLK2 :
-
D14-LIKE2
- KUF1 :
-
KAR-UP F-BOX1
- IAA1 :
-
INDOLE-3-ACETIC ACID INDUCIBLE1
References
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117. doi:10.1093/pcp/pcq058
Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-Carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351. doi:10.1126/science.1218094
Bythell-Douglas R, Waters MT, Scaffidi A, Flematti GR, Smith SM, Bond CS (2013) The structure of the karrikin-insensitive protein (KAI2) in Arabidopsis thaliana. PLoS One 8:e54758. doi:10.1371/journal.pone.0054758
Cardoso C, Charnikhova T, Jamil M, Delaux PM, Verstappen F, Amini M, Lauressergues D, Ruyter-Spira C, Bouwmeester H (2014) Differential activity of Striga hermonthica seed germination stimulants and Gigaspora rosea hyphal branching factors in rice and their contribution to underground communication. PLoS One 9:e104201. doi:10.1371/journal.pone.0104201
Conn CE, Nelson DC (2015) Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front Plant Sci 6:1219. doi:10.3389/fpls.2015.01219
Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B et al (2015) Plant evolution. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:540–543. doi:10.1126/science.aab1140
Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977
Flematti GR, Waters MT, Scaffidi A, Merritt DJ, Ghisalberti EL, Dixon KW, Smith SM (2013) Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds. Mol Plant 6:29–37. doi:10.1093/mp/sss132
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194
Guo Y, Zheng Z, La Clair J, Chory J, Noel J (2013) Smoke-derived karrikin perception by the α/β-hydrolase KAI2 from Arabidopsis. Proc Natl Acad Sci USA 110:8284–8289. doi:10.1073/pnas.1306265110
Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 Is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22:2032–2036. doi:10.1016/j.cub.2012.08.007
Jia KP, Luo Q, He SB, Lu XD, Yang HQ (2014) Strigolactone-regulated hypocotyl elongation is dependent on cryptochrome and phytochrome signaling pathways in Arabidopsis. Mol Plant 7:528–540. doi:10.1093/mp/sst093
Jiang L, Liu X, Xiong GS, Liu HH, Chen FL et al (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:401–405. doi:10.1038/nature12870
Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, Seto Y, Yamaguchi S, Hakoshima T et al (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells. doi:10.1111/gtc.12025
Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S et al (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216. doi:10.1007/s00425-010-1310-y
Lauressergues D, André O, Peng JL, Wen JQ, Chen RJ et al (2014) Strigolactones contribute to shoot elongation and to the formation of leaf margin serrations in Medicago truncatula R108. J Exp Bot 66:1237–1244. doi:10.1093/jxb/eru471
Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X et al (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613. doi:10.1038/ncomms3613
Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon KW, Smith SM (2009) Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol 149:863–873. doi:10.1104/pp.108.131516
Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Smith SM (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:7095–7100. doi:10.1073/pnas.0911635107
Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR et al (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:8897–8902. doi:10.1073/pnas.1100987108
Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM (2012) Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu Rev Plant Biol 63:107–130. doi:10.1146/annurev-arplant-042811-105545
Rasmussen A, Mason MG, De Cuyper C, Brewer PB et al (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158:1976–1987. doi:10.1104/pp.111.187104
Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734. doi:10.1104/pp.110.166645
Scaffidi A, Waters MT, Ghisalberti EL, Dixon KW, Flematti GR, Smith SM (2013) Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J 76:1–9. doi:10.1111/tpj.12265
Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:1221–1232. doi:10.1104/pp.114.240036
Sessions A, Burke E, Presting G, Aux G, McElver J et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994
Seto Y, Yamaguchi S (2014) Strigolactone biosynthesis and perception. Curr Opin Plant Biol 21C:1–6. doi:10.1016/j.pbi.2014.06.001
Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci USA 111:1640–1645. doi:10.1073/pnas.1314805111
Shen H, Luong P, Huq E (2007) The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol 145:1471–1483
Shen H, Zhu L, Bu QY, Huq E (2012) MAX2 affects multiple hormones to promote photomorphogenesis. Mol Plant 5:750–762. doi:10.1093/mp/sss029
Soundappan I, Bennett T, Morffy N, Liang YY, Stanga JP, Abbas A, Leyser O, Nelson DC (2015) SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27:3143–3159. doi:10.1105/tpc.15.00562
Stanga JP, Smith SM, Briggs WR, Nelson DC (2013) SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol 163:318–330. doi:10.1104/pp.113.221259
Stirnberg P, Furner IJ, Ottoline Leyser HM (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94
Sun H, Tao J, Hou M, Huang S, Chen S, Liang Z et al (2015) A strigolactone signal is required for adventitious root formation in rice. Ann Bot 115:1155–1162. doi:10.1093/aob/mcv052
Toh S, Holbrook-Smith D, Stokes ME, Tsuchiya Y, McCourt P (2014) Detection of parasitic plant suicide germination compounds using a high-throughput Arabidopsis HTL/KAI2 strigolactone perception system. Chem Biol 21:988–998. doi:10.1016/j.chembiol.2014.07.005
Toh S, Holbrook-Smith D, Stogios PJ, Onopriyenki O, Lumba S et al (2015) Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350:203–207
Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt PM (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6:741–749. doi:10.1038/nchembio.435
Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S et al (2015) Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:864–868. doi:10.1126/science.aab3831
Ueda H, Kusaba M (2015) Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 169:138–147. doi:10.1104/pp.15.00325
Umehara M, Hanada A, Yoshida S, Akiyama K et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200
Umehara M, Cao MM, Akiyama K, Akatsu T et al (2015) Structural requirements of strigolactones for shoot branching inhibition in rice and Arabidopsis. Plant Cell Physiol 56:1059–1072. doi:10.1093/pcp/pcv028
Wang L, Wang B, Jiang L, Liu X, Li XL, Lu ZF et al (2015) Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27:3128–3142. doi:10.1105/tpc.15.00605
Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139:1285–1295. doi:10.1242/dev.074567
Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM (2014) The karrikin response system of Arabidopsis. Plant J 79:623–631. doi:10.1111/tpj.12430
Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM (2015) A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27:1925–1944. doi:10.1105/tpc.15.00146
Xie X, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117. doi:10.1146/annurev-phyto-073009-114453
Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:399–408. doi:10.1007/s00425-014-2096-0
Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494
Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, Li S, Xu TH et al (2013) Crystal structures of two phytohormone signal-transducing alpha/beta hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23:436–439. doi:10.1038/cr.2013.19
Zhao J, Wang T, Wang MX, Liu YY, Yuan SJ et al (2014) DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol 55:1096–1109. doi:10.1093/pcp/pcu045
Zhao LH, Zhou XE, Yi W, Wu Z, Liu Y et al (2015) Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res 25:1219–1236. doi:10.1038/cr.2015.122
Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N et al (2013) D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410. doi:10.1038/nature12878
Acknowledgments
Funding from the National Science Foundation (IOS-1350561) to D.C.N. and NIGMS National Institutes of Health Award T32GM007103 to N.M. supported this work.
Author information
Authors and Affiliations
Corresponding author
Additional information
A contribution to the special issue on Strigolactones.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Stanga, J.P., Morffy, N. & Nelson, D.C. Functional redundancy in the control of seedling growth by the karrikin signaling pathway. Planta 243, 1397–1406 (2016). https://doi.org/10.1007/s00425-015-2458-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-015-2458-2