Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds

Molecular Plant

Volumn 6, Issue 1, 2013, Pages 29-37

  Flematti, Gavin R ^a   Waters, Mark T ^a   Scaffidi, Adrian ^a   Merritt, David J ^a,b   Ghisalberti, Emilio L ^a   Dixon, Kingsley W ^a,b   Smith, Steven M ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b KINGS PARK AND BOTANIC GARDEN   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3-METHYL-2H-FURO(2,3-C)PYRAN-2-ONE; CYANOHYDRIN; FURAN DERIVATIVE; NITRILE; PYRAN DERIVATIVE; SMOKE;

CHEMISTRY; METABOLISM; PLANT; PLANT DEVELOPMENT; SIGNAL TRANSDUCTION; SMOKE;

FURANS; NITRILES; PLANT DEVELOPMENT; PLANTS; PYRANS; SIGNAL TRANSDUCTION; SMOKE;

EID: 84875698895     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss132     Document Type: Review

References (80)

1. Agusti, J., Herold, S., Schwarz, M., Sanchez, P., Ljung, K., Dun, E.A., Brewer, P.B., Beveridge, C.A., Sieberer, T., Sehr, E.M., et al. (2011). Strigolactone signalling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl Acad. Sci. U S A. 108, 20242-20247.
2. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 435, 824-827.
3. Amasino, R. (2005). 1955: kinetin arrives: the 50th anniversary of a new plant hormone. Plant Physiol. 138, 1177-1184.
4. Baldwin, I.T., Staszak-Kozinski, L., and Davidson, R. (1994). Up in smoke: I. Smoke-derived germination cues for postfire annual, Nicotiana attenuata Torr. Ex. Watson. J. Chem. Ecol. 20, 2345-2371.
5. Bethke, P.C., Libourel, I.G.L., Reinohl, V., and Jones, R.L. (2006). Sodium nitroprusside, cyanide, nitrite and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta. 223, 805-812.
6. Bisson, M.M.A., and Groth, G. (2012). Cyanide is an adequate agonist of the plant hormone ethylene for studying signalling of sensor kinase ETR1 at the molecular level. Biochem. J. 444, 261-267.
7. Bogatek, R., Dziewanowska, K., and Lewak, S. (1991). Hydrogencyanide and embryonal dormancy in apple seeds. Physiol. Plant. 83, 417-421.
8. Bradshaw, S.D., Dixon, K.W., Hopper, S.D., Lambers, H., and Turner, S.R. (2011). Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci. 16, 69-76.
9. Brase, S., Encinas, A., Keck, J., and Nising, C.F. (2009). Chemistry and biology of mycotoxins and related fungal metabolites. Chem. Rev. 109, 3903-3990.
10. Brown, N.A.C., and van Staden, J. (1997). Smoke as a germination cue: a review. Plant Growth Regul. 22, 115-124.
11. Chivasa, S., and Carr, J.P. (1998). Cyanide restores N gene-mediated resistance to tobacco mosaic virus in transgenic tobacco expressing salicylic acid hydroxylase. Plant Cell. 10, 1489-1498.
12. Chiwocha, S.D.S., Dixon, K.W., Flematti, G.R., Ghisalberti, E.L., Merritt, D.J., Nelson, D.C., Riseborough, J.M., Smith, S.M., and Stevens, J.C. (2009). Karrikins: a new family of plant growth regulators in smoke. Plant Sci. 177, 252-256.
13. Cohn, M.A., and Hughes, J.A. (1986). Seed dormancy in red rice. 5. Response to azide, hydroxylamine and cyanide. Plant Physiol. 80, 531-533.
14. Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E., and Egley, G.H. (1966). Germination of witchweed (Strigalutea Lour.): isolation and properties of a potent stimulant. Science. 154, 1189-1190.
15. Cook, C.E., Whichard, L.P., Wall, M.E., Egley, G.H., Coggon, P., Luhan, P.A., and McPhail, A.T. (1972). Germination stimulants. II. The structure of strigola potent seed germination stimulant for witchweed (Striga lutea Lour.). J. Am. Chem. Soc. 94, 6198-6199.
16. Daws, M.I., Pritchard, H.W., and Van Staden, J. (2008). Butenolide from plant-derived smoke functions as a strigolactone analogue: evidence from parasitic weed seed germination. S. Afr. J. Bot. 74, 116-120.
17. De Lange, J.H., and Boucher, C. (1990). Autecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. S. Afr. J. Bot. 56, 700-703.
18. Delaux, P.M., Xie, X., Timme, R.E., Puech-Pages, V., Dunand, C., Lecompte, E., Delwiche, C.F., Yoneyama, K., Becard, G., and Sejalon-Delmas, N. (2012). Origin of strigolactones in the green lineage. New Phytol. 195, 857-871.
19. Dixon, K.W., Merritt, D.J., Flematti, G.R., and Ghisalberti, E.L. (2009). Karrikinolide-a phytoreactive compound derived from smoke with applications in horticulture, ecological restoration and agriculture. Acta Hortic. 813, 155-170.
20. Doubt, S.L. (1917). The response of plants to illuminating gas. Botanical Gazette. 63, 209-224.
21. Downes, K.S., Lamont, B.B., Light, M.E., and van Staden, J. (2010). The fire ephemeral Tersonia cyathiflora (Gyrostemonaceae) germinates in response to smoke but not the butenolide 3-methyl-2H-furo[2, 3-c]pyran-2-one. Ann. Bot. 106, 381-384.
22. Drewes, F.E., Smith, M.T., and van Staden, J. (1995). The effect of a plant derived smoke extract on the germination of lightsensitive lettuce seed. Plant Growth Regul. 16, 205-209.
23. Esashi, Y., Isuzugawa, K., Matsuyama, S., Ashino, H., and Hasegawa, R. (1991). Endogenous evolution of HCN during pre-germination periods in many seed species. Physiol. Plant. 83, 27-33.
24. Evidente, A., Fernandez-Aparicio, M., Cimmino, A., Rubiales, D., Andolfi, A., and Motta, A. (2009). Peagol and peagoldione, two new strigolactone-like metabolites isolated from pea root exudates. Tetrahedron Lett. 50, 6955-6958.
25. Flematti, G.R., Ghisalberti, E.L., Dixon, K.W., and Trengove, R.D. (2004). A compound from smoke that promotes seed germination. Science. 305, 977.
26. Flematti, G.R., Ghisalberti, E.L., Dixon, K.W., and Trengove, R.D. (2005). Synthesis of the seed germination stimulant 3-methyl- 2H-furo[2, 3-c]pyran-2-one. Tetrahedron Lett. 46, 5719-5721.
27. Flematti, G.R., Ghisalberti, E.L., Dixon, K.W., and Trengove, R.D. (2009). Identification of alkyl substituted 2H-furo[2, 3-c]pyran- 2-ones as germination stimulants present in smoke. J. Agric. Food Chem. 57, 9475-9480.
28. Flematti, G.R., Merritt, D., J., Piggott, M.J., Trengove, R.D., Smith, S.M., Dixon, K., W., and Ghisalberti, E.L. (2011). Burning vegetation produces cyanohydrins that liberate cyanide and promote seed germination. Nat. Commun. 2, 360.
29. Fol, M., Frachise, J.M., Petel, G., and Gendraud, M. (1989). Effect of cyanide on the membrane-potential of Jerusalem artichoke (Helianthus tuberosus L) tuber-parenchyma: different responses in relation to dormancy. C. R. Acad. Sci. III, Sci. Vie. 309, 551-556.
30. Gane, R. (1934). Production of ethylene by some fruits. Nature. 134, 1008.
31. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pagès, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., et al. (2008). Strigolactone inhibition of shoot branching. Nature. 455, 189-194.
32. Grossmann, K. (1996). A role for cyanide, derived from ethylene biosynthesis, in the development of stress symptoms. Physiol. Plant. 97, 772-775.
33. Hamiaux, C., Drummond, R.S.M., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D., and Snowden, K.C. (2012). DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 22, 2032-2036.
34. Hendricks, S.B., and Taylorson, R.B. (1972). Promotion of seed germination by nitrates and cyanides. Nature. 237, 169-170.
35. Hughes, J., Smith, T.W., Kosterlitz, H.W., Fothergill, L.A., Morgan, B.A., and Morris, H.R. (1975). Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature. 258, 577-580.
36. Iwai, T., Miyasaka, A., Seo, S., and Ohashi, Y. (2006). Contribution of ethylene biosynthesis for resistance to blast fungus infection in young rice plants. Plant Physiol. 142, 1202-1215.
37. Joel, D.M., Chaudhuri, S.K., Plakhine, D., Ziadna, H., and Steffens, J.C. (2011). Dehydrocostus lactone is exuded from sunflower roots and stimulates germination of the root parasite Orobanche cumana. Phytochemistry. 72, 624-634.
38. Kapulnik, Y., Delaux, P.M., Resnick, N., Mayzlish-Gati, E., Wininger, S., Bhattacharya, C., Sejalon-Delmas, N., Combier, J.P., Becard, G., Belausov, E., et al. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta. 233, 209-216.
39. Kato, T., Kabuto, C., Sasaki, N., Tsunagaw, M, Aizawa. H., Fujita, K., Kato, Y., and Kitahara, Y. (1973). Momilactones, growth inhibitors from rice, Oryza-sativa L. Tetrahedron Lett. 14, 3861-3864.
40. Keeley, J.E., Morton, B.A., Pedrosa, A., and Trotter, P. (1985). Role of allelopathy, heat and charred wood in the germination of chaparral herbs and suffrutescents. J. Ecol. 73, 445-458.
41. Knight, D.W. (1994). Synthetic approaches to butenolides. Contemp. Org. Synth. 1, 287-315.
42. Letham, D.S., and Miller, C.O. (1965). Identity of kinetin-like factors from Zea mays. Plant Cell Physiol. 6, 355-359.
43. Major, W., and Roberts, E.H. (1968). Dormancy in cereal seeds. I. The effects of oxygen and respiratory inhibitors. J. Exp. Bot. 19, 77-89.
44. McMahon Smith, J., and Arteca, R.N. (2000). Molecular control of ethylene production by cyanide in Arabidopsis thaliana. Physiol. Plant. 109, 180-187.
45. Mennan, H., Ngouajio, M., Sahin, M., Isik, D., and Altop, E.K. (2012). Quantification of momilactone B in rice hulls and the phytotoxic potential of rice extracts on the seed germination of Alisma plantago-aquatica. Weed Biology and Management. 12, 29-39.
46. Miller, C.O., Skoog, F., Von Saltza, M.H., and Strong, F. (1955). Kinetin, a cell division factor from deoxyribonucleic acid. J. Am. Chem. Soc. 77, 1392.
47. Mithöfer, A., and Boland, W. (2012). Plant defense against herbivors: chemical aspects. Annu. Rev. Plant Biol. 63, 431-450.
48. Negishi, E., and Kotora, M. (1997). Regio- and stereoselective synthesis of gamma-alkylidenebutenolides and related compounds. Tetrahedron. 53, 6707-6738.
49. Nelson, D.C., Flematti, G.R., Ghisalberti, E.L., Dixon, K.W., and Smith, S.M. (2012). Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu. Rev. Plant Biol. 63, 107-130.
50. Nelson, D.C., Riseborough, J.A., Flematti, G.R., Stevens, J., Ghisalberti, E.L., Dixon, K.W., and Smith, S.M. (2009). Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol. 149, 863-873.
51. Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A., Ghisalberti, E.L., and Smith, S.M. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone signalling in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 108, 8897-8902.
52. Nielsen, K.A., Olsen, C.E., Pontoppidan, K., and Moller, B.L. (2002). Leucine-derived cyano glucosides in barley. Plant Physiol. 129, 1066-1075.
53. Okrob, D., Paravidino, M., Orru, R.V.A., Wiechert, W., Hanefeld, U., and Pohl, M. (2011). Hydroxynitrile lyase from Arabidopsis thaliana: identification of reaction parameters for enantiopure cyanohydrin synthesis by pure and immobilized catalyst. Adv. Synth. Catal. 353, 2399-2408.
54. Oracz, K., El-Maarouf-Bouteau, H., Bogatek, R., Corbineau, F., and Bailly, C. (2008). Release of sunflower seed dormancy by cyanide: cross-talk with ethylene signalling pathway. J. Exp. Bot. 59, 2241-2251.
55. Oracz, K., El-Maarouf-Bouteau, H., Kranner, I., Bogatek, R., Corbineau, F., and Bailly, C. (2009). The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signalling during germination. Plant Physiol. 150, 494-505.
56. Oracz, K., El-Maarouf-Bouteau, H., Farrant, J.M., Cooper, K., Belghazi, M., Job, C., Job, D., Corbineau, F., and Bailly, C. (2007). ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J. 50, 452-465.
57. Peiser, G.D., Wang, T.T., Hoffman, N.E., Yang, S.F., Liu, H.W., and Walsh, C.T. (1984). Formation of cyanide from carbon 1 of 1-aminocyclopropane-1- carboxylic acid during its conversion to ethylene. Proc. Natl Acad. Sci. U S A. 81, 3059-3063.
58. Preston, C.A., Becker, R., and Baldwin, I.T. (2004). Is 'NO' news good news? Nitrogen oxides are not components of smoke that elicits germination in two smoke-stimulated species, Nicotiana attenuata and Emmenanthe penduliflora. Seed Sci. Res. 14, 73-79.
59. Rasmussen, A., Beveridge, C.A., and Geelen, D. (2012). Inhibition of strigolactones promotes adventitious root formation. Plant Signal. Behav. 7, 694-697.
60. Roche, S., Dixon, K.W., and Pate, J.S. (1997a). Seed ageing and smoke: partner cues in the amelioration of seed dormancy in selected Australian native species. Aust. J. Bot. 45, 783-815.
61. Roche, S., Koch, J.M., and Dixon, K.W. (1997b). Smoke enhanced seed germination for mine rehabilitation in the southwest of Western Australia. Restor. Ecol. 5, 191-203.
62. Ruyter-Spira, C., Kohlen, W., Charnikhova, T., van Zeijl, A., van Bezouwen, L., de Ruijter, N., Cardoso, C., Lopez-Raez, J.A., Matusova, R., Bours, R., et al. (2011). Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another below ground role for strigolactones? Plant Physiol. 155, 721-734.
63. Scaffidi, A., Flematti, G.R., Nelson, D.C., Dixon, K.,W., Smith, S.M., and Ghisalberti, E.L. (2012). Insight into the molecular mechanism of karrikins and strigolactones, Bioorg. Med. Chem. Lett. 22, 3743-3746.
64. Seigler, D. (1998). Cyanogenic glycosides and cyanolipids. In Plant Secondary Metabolism, Seigler, D., ed. (Norwell, MA: Kluwer Academic Press), pp. 273-299.
65. Shen, H., Luong, P., and Huq, E. (2007). The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol. 145, 1471-1483.
66. Siegien, I., and Bogatek, R. (2006). Cyanide action in plants-from toxic to regulatory. Acta Physiol. Plant. 28, 483-497.
67. Smith, C.J., Perfetti, T.A., Garg, R., and Hansch, C. (2003). IARC carcinogens reported in cigarette mainstream smoke and their calculated log P values. Food Chem. Toxicol. 41, 807-817.
68. Smith, S.M., and Waters, M.T. (2012). Strigolactones: destructiondependent perception? Curr. Biol. 22, R924-R927.
69. Takahashi, N. (1998). Discovery of gibberellin. In Discoveries in Plant Biology, Kung, S.D., and Yang, S.F., eds (Singapore: World Scientific Publishing Co.), pp. 17-32.
70. Thomas, T.H., and Van Staden, J. (1995). Dormancy break of celery (Apium graveolens L.) seeds by plant derived smoke extract. Plant Growth Regul. 17, 195-198.
71. Ueda, M., and Nakamura, Y. (2006). Metabolites involved in plant movement and 'memory': nyctinasty of legumes and trap movement in the Venus flytrap. Nat. Prod. Rep. 23, 548-557.
72. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., et al. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature. 455, 195-200.
73. Van Staden, J., Brown, N.A.C., Jäger, A.K., and Johnson, T.A. (2000). Smoke as a germination cue. Plant Species Biol. 15, 167-178.
74. Wang, K.L., Li, H., and Ecker, J.R. (2002). Ethylene biosynthesis and signalling networks. Plant Cell. 14 Suppl., S131-S151.
75. Waters, M.T., and Smith, S.M. (2013). KAI2- and MAX2-mediated responses to karrikins and strigolactones are largely independent of HY5 in Arabidopsis seedlings. Mol. Plant. 6, 62-74.
76. Waters, M.T., et al. (2012a). Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development. 139, 1285-1295.
77. Waters, M.T., Scaffidi, A., Flematti, G.R., and Smith, S.M. (2012b). Karrikins force a rethink of strigolactone mode of action. Plant Signal. Behav. 7, 969-972.
78. Wong, C.E., Carson, R.A., and Carr, J.P. (2002). Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. Mol. Plant-Microbe Interact. 15, 75-81.
79. Woo, H.R., Chung, K.M., Park, J.H., Oh, S.A., Ahn, T., Hong, S.H., Jang, S.K., and Nam, H.G. (2001). ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell. 13, 1779-1790.
80. Yoneyama, K., Xie, X., Kim, H.I., Kisugi, T., Nomura, T., Sekimoto, H., and Yokota, T. (2012). How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta. 235, 1197-1207.