Smoke and Hormone Mirrors: Action and Evolution of Karrikin and Strigolactone Signaling

Trends in Genetics

Volumn 32, Issue 3, 2016, Pages 176-188

  Morffy, Nicholas ^a   Faure, Lionel ^a   Nelson, David C ^a  

^a University of Georgia   (United States)

Author keywords

Branching; Germination; Hormones; Parasitism; Proteolysis

Indexed keywords

AUXIN; BUTENOLIDE; D14 PROTEIN; F BOX PROTEIN; GIBBERELLIN; HYDROLASE; JASMONIC ACID; KAI2 PROTEIN; KARRIKIN; MAX2 PROTEIN; PHYTOHORMONE; PROTEASOME; SMXL PROTEIN; STRIGOLACTONE; UNCLASSIFIED DRUG; 3-METHYL-2H-FURO(2,3-C)PYRAN-2-ONE; FURAN DERIVATIVE; LACTONE; PYRAN DERIVATIVE;

GENE; GENE DUPLICATION; KAI2 GENE; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FAMILY; REVIEW; SIGNAL TRANSDUCTION; SMOKE; METABOLISM;

FURANS; LACTONES; PYRANS; SIGNAL TRANSDUCTION;

EID: 84958780056     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2016.01.002     Document Type: Review

References (85)

1. 2H-Furo[2,3-c]pyran-2-ones as germination stimulants present in smoke. J. Agric. Food Chem. 2009, 57:9475-9480.
2. Flematti G.R., et al. A compound from smoke that promotes seed germination. Science 2004, 305:977.
3. Nelson D.C., et al. Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu. Rev. Plant Biol. 2012, 63:107-130.
4. Nelson D.C., et al. Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7095-7100.
5. Nelson D.C., et al. Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol. 2009, 149:863-873.
6. H-furo[2,3-c]pyran-2-one, and its potential as a preconditioning agent. Field Crops Res. 2006, 98:98-105.
7. Kulkarni M.G., et al. Stimulation of rice (Oryza sativa L.) seedling vigour by smoke-water and butenolide. J. Agron. Crop Sci. 2006, 192:395-398.
8. Jain N., et al. A butenolide, isolated from smoke, can overcome the detrimental effects of extreme temperatures during tomato seed germination. Plant Growth Regul. 2006, 49:263-267.
9. Cook C.E., et al. Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 1966, 154:1189-1190.
10. Akiyama K., et al. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435:824-827.
11. Gomez-Roldan V., et al. Strigolactone inhibition of shoot branching. Nature 2008, 455:189-194.
12. Kohlen W., et al. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol. 2012, 196:535-547.
13. Umehara M., et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature 2008, 455:195-200.
14. Kapulnik Y., et al. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 2011, 233:209-216.
15. Ruyter-Spira C., et al. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones?. Plant Physiol. 2011, 155:721-734.
16. Rasmussen A., et al. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 2012, 158:1976-1987.
17. Stirnberg P., et al. MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 2002, 129:1131-1141.
18. Lauressergues D., et al. Strigolactones contribute to shoot elongation and to the formation of leaf margin serrations in Medicago truncatula R108. J. Exp. Bot. 2015, 66:1237-1244.
19. Scaffidi A., et al. Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J. 2013, 76:1-9.
20. Ueda H., Kusaba M. Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol. 2015, 169:138-147.
21. Yamada Y., et al. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 2014, 240:399-408.
22. Agusti J., et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:20242-20247.
23. Zhang Y., et al. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 2014, 10:1028-1033.
24. Seto Y., et al. Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:1640-1645.
25. Abe S., et al. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:18084-18089.
26. Waters M.T., et al. The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol. 2012, 159:1073-1085.
27. Alder A., et al. The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 2012, 335:1348-1351.
28. Lin H., et al. DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 2009, 21:1512-1525.
29. Kretzschmar T., et al. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 2012, 483:341-344.
30. Sasse J., et al. Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Curr. Biol. 2015, 25:647-655.
31. Fridlender M., et al. Influx and efflux of strigolactones are actively regulated and involve the cell-trafficking system. Mol. Plant 2015, 8:1809-1812.
32. Nelson D.C., et al. F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:8897-8902.
33. Arite T., et al. d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 2009, 50:1416-1424.
34. Waters M.T., et al. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 2012, 139:1285-1295.
35. Hamiaux C., et al. DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 2012, 22:2032-2036.
36. Shen H., et al. MAX2 affects multiple hormones to promote photomorphogenesis. Mol. Plant 2012, 5:750-762.
37. Scaffidi A., et al. Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 2014, 165:1221-1232.
38. Soundappan I., et al. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 2015, 27:3143-3159.
39. Umehara M., et al. Structural requirements of strigolactones for shoot branching inhibition in rice and Arabidopsis. Plant Cell Physiol. 2015, 56:1059-1072.
40. Zhao L.H., et al. Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res. 2015, 25:1219-1236.
41. Kameoka H., Kyozuka J. Downregulation of rice DWARF 14 LIKE suppress mesocotyl elongation via a strigolactone independent pathway in the dark. J. Genet. Genomics 2015, 42:119-124.
42. Kagiyama M., et al. Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 2013, 18:147-160.
43. Nakamura H., et al. Molecular mechanism of strigolactone perception by DWARF14. Nat. Commun. 2013, 4:2613.
44. Zhao L.H., et al. Crystal structures of two phytohormone signal-transducing alpha/beta hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res. 2013, 23:436-439.
45. Chevalier F., et al. Strigolactone promotes degradation of DWARF14, an alpha/beta hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 2014, 26:1134-1150.
46. Guo Y., et al. Smoke-derived karrikin perception by the α/β-hydrolase KAI2 from Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:8284-8289.
47. Waters M.T., et al. A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 2015, 27:1925-1944.
48. Waters M.T., et al. Substrate-induced degradation of the alpha/beta-fold hydrolase KARRIKIN INSENSITIVE2 requires a functional catalytic triad but is independent of MAX2. Mol. Plant 2015, 8:814-817.
49. Waters M.T., et al. The karrikin response system of Arabidopsis. Plant J. 2014, 79:623-631.
50. Conn C.E., et al. PLANT EVOLUTION. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 2015, 349:540-543.
51. Tsuchiya Y., et al. PARASITIC PLANTS. Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 2015, 349:864-868.
52. Toh S., et al. Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 2015, 350:203-207.
53. Somers D.E., Fujiwara S. Thinking outside the F-box: novel ligands for novel receptors. Trends Plant Sci. 2009, 14:206-213.
54. Stirnberg P., et al. MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J. 2007, 50:80-94.
55. Zhao J., et al. DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol. 2014, 55:1096-1109.
56. Gray W.M., et al. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 2001, 414:271-276.
57. Thines B., et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 2007, 448:661-665.
58. Chini A., et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007, 448:666-671.
59. Tan X., et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 2007, 446:640-645.
60. Sheard L.B., et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 2010, 468:400-405.
61. Murase K., et al. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 2008, 456:459-463.
62. Hauvermale A.L., et al. Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol. 2012, 160:83-92.
63. Stanga J.P., et al. SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 2013, 163:318-330.
64. Jiang L., et al. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 2013, 504:401-405.
65. Zhou F., et al. D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 2013, 504:406-410.
66. Wang L., et al. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 2015, 27:3128-3142.
67. Yoneyama K., et al. Strigolactones as germination stimulants for root parasitic plants. Plant Cell Physiol. 2010, 51:1095-1103.
68. Delaux P.M., et al. Origin of strigolactones in the green lineage. New Phytol. 2012, 195:857-871.
69. Flematti G.R., et al. Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds. Mol. Plant 2013, 6:29-37.
70. Conn C.E., Nelson D.C. Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front. Plant Sci. 2016, 6:1219.
71. Proust H., et al. Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 2011, 138:1531-1539.
72. Hoffmann B., et al. Strigolactones inhibit caulonema elongation and cell division in the moss Physcomitrella patens. PLoS ONE 2014, 9:e99206.
73. Gutjahr C., et al. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 2015, 350:1521-1524.
74. Yoshida S., et al. The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol. 2012, 196:1208-1216.
75. Flematti G.R., et al. Production of the seed germination stimulant karrikinolide from combustion of simple carbohydrates. J. Agric. Food Chem. 2011, 59:1195-1198.
76. Xie X., et al. Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol. Plant 2013, 6:153-163.
77. Challis R.J., et al. A role for more axillary growth1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol. 2013, 161:1885-1902.
78. Long J.A., et al. TOPLESS regulates apical embryonic fate in Arabidopsis. Science 2006, 312:1520-1523.
79. Krogan N.T., et al. APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 2012, 139:4180-4190.
80. Szemenyei H., et al. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 2008, 319:1384-1386.
81. Pauwels L., et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 2010, 464:788-791.
82. Causier B., et al. The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol. 2012, 158:423-438.
83. Shyu C., et al. JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis. Plant Cell 2012, 24:536-550.
84. Mashiguchi K., et al. Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci. Biotechnol. Biochem. 2009, 73:2460-2465.
85. Ke J., et al. Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors. Sci. Adv. 2015, 1:e1500107.