Apical dominance in saffron and the involvement of the branching enzymes CCD7 and CCD8 in the control of bud sprouting

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Rubio Moraga, Angela ^a   Ahrazem, Oussama ^a,b   Pérez Clemente, Rosa M ^c   Gómez Cadenas, Aurelio ^c   Yoneyama, Koichi ^d   López Ráez, Juan A ^e   Molina, Rosa V ^f   Gómez Gómez, Lourdes ^a  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b Instituto de Recursos Humanos Para la Ciencia y la Tecnología INCRECYT FEDER Fundación Parque Científico y Tecnológico de Albacete   (Spain)

^c UNIVERSITAT JAUME I   (Spain)

^d UTSUNOMIYA UNIVERSITY   (Japan)

^e CSIC   (Spain)

^f UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

Auxin; Buds; Carotenoid cleavage oxygenases; Corm; Saffron; Strigolactones

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; LACTONE; MESSENGER RNA; PHYTOHORMONE; VEGETABLE PROTEIN;

BIOASSAY; CROCUS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT GENE;

1,4-ALPHA-GLUCAN BRANCHING ENZYME; BIOLOGICAL ASSAY; CROCUS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GERMINATION; LACTONES; MERISTEM; PHYLOGENY; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT SHOOTS; RNA, MESSENGER;

EID: 84902758874     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-171     Document Type: Article

References (94)

1. Rubio-Moraga A, Trapero A, Ahrazem O, Gomez-Gomez L. Crocins transport in Crocus sativus: the long road from a senescent stigma to a newborn corm. Phytochemistry 2010, 71(13):1506-1513.
2. Hosseinzadeh H, Nassiri-Asl M. Avicenna's (Ibn Sina) the canon of medicine and saffron (Crocus sativus): a review. Phytother Res 2013, 27(4):475-483.
3. Moraga AR, Rambla JL, Ahrazem O, Granell A, Gomez-Gomez L. Metabolite and target transcript analyses during Crocus sativus stigma development. Phytochemistry 2009, 70(8):1009-1016.
4. Molina RV, Valero M, Navarro Y, Guardiola JL, García-Luis A. Temperature effects on flower formation in saffron (Crocus sativus L. Sci Hortic 2005, 103:18.
5. Renau-Morata B, Moyá L, Nebauer SG, Seguí-Simarro JM, Parra-Vega V, Gómez MD, Molina RV. The use of corms produced under storage at low temperatures as a source of explants for the in vitro propagation of saffron reduces contamination levels and increases multiplication Industrial. Crops Products 2013, 46:7.
6. Chrungoo NK. Concepts of dormancy regulation in vegetative plant propagules: a review. Environ Exp Bot 1992, 32(4):9.
7. Ahrazem O, Rubio-Moraga A, Trapero A, Gomez-Gomez L. Developmental and stress regulation of gene expression for a 9-cis-epoxycarotenoid dioxygenase, CstNCED, isolated from Crocus sativus stigmas. J Exp Bot 2012, 63(2):681-694.
8. Farooq S, Koul KK. Changes in Gibberellin-like activity in corms of saffron plant (Crocus sativus L.) during dormancy and sprouting. Biochem Physiol Pflanz 1983, 178(8):5.
9. Aguilar-Martinez JA, Poza-Carrion C, Cubas P. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 2007, 19(2):458-472.
10. Shimizu-Sato S, Mori H. Control of outgrowth and dormancy in axillary buds. Plant Physiol 2001, 127(4):1405-1413.
11. Brewer PB, Koltai H, Beveridge CA. Diverse roles of strigolactones in plant development. Mol Plant 2013, 6(1):18-28.
12. 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):553-563.
13. Stirnberg P, van De Sande K, Leyser HM. MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 2002, 129(5):1131-1141.
14. Liang J, Zhao L, Challis R, Leyser O. Strigolactone regulation of shoot branching in chrysanthemum (Dendranthema grandiflorum). J Exp Bot 2010, 61(11):3069-3078.
15. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA. Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 2009, 150(1):482-493.
16. Ferguson BJ, Beveridge CA. Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 2009, 149(4):1929-1944.
17. Cook C, Coggon P, McPhail A, Wall M, Whichard L, Egley G, Luhan P. Germination stimulants. 2. Structure of strigol - potent seed-germination stimulant for witchweed (Striga lutea Lour). J Am Chem Society 1972, 94:2.
18. Akiyama K, Matsuzaki K, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 435(7043):824-827.
19. Yoneyama K, Xie X, Takeuchi Y. Strigolactones: structures and biological activities. Pest Manag Sci 2009, 65(5):467-470.
20. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF. Strigolactone inhibition of shoot branching. Nature 2008, 455(7210):189-194.
21. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S. Inhibition of shoot branching by new terpenoid plant hormones. Nature 2008, 455(7210):195-200.
22. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H. The biology of strigolactones. Trends Plant Sci 2013, 18(2):72-83.
23. Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Sejalon-Delmas N, Combier JP, Becard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 2011, 233(1):209-216.
24. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge CA. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 2012, 158(4):1976-1987.
25. Kohlen W, Charnikhova T, Lammers M, Pollina T, Toth P, Haider I, Pozo MJ, de Maagd RA, Ruyter-Spira C, Bouwmeester HJ, López-Ráez JA. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 2012, 196(2):535-547.
26. Yoneyama K, Takeuchi Y, Sekimoto H. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 2007, 225(4):1031-1038.
27. Lopez-Raez JA, Bouwmeester H. Fine-tuning regulation of strigolactone biosynthesis under phosphate starvation. Plant Signal Behav 2008, 3(11):963-965.
28. Ha CV, Leyva-Gonzalez MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Dong NV, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LS. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci U S A 2013, 111(2):851-856.
29. Aroca R, Ruiz-Lozano JM, Zamarreno AM, Paz JA, Garcia-Mina JM, Pozo MJ, Lopez-Raez JA. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 2013, 170(1):47-55.
30. Torres-Vera R, Garcia JM, Pozo MJ, Lopez-Raez JA. Do strigolactones contribute to plant defence?. Mol Plant Pathol 2013, 15(2):211-216.
31. Beveridge CA, Ross JJ, Murfet IC. Branching Mutant rms-2 in Pisum sativum (Grafting Studies and Endogenous Indole-3-Acetic Acid Levels). Plant Physiol 1994, 104(3):953-959.
32. Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O. MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 2003, 17(12):1469-1474.
33. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S. The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 2012, 335(6074):1348-1351.
34. Challis RJ, Hepworth J, Mouchel C, Waites R, Leyser O. A role for more axillary growth1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol 2013, 161(4):1885-1902.
35. Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S. Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci U S A 2014, 111(4):1640-1645.
36. Morris SE, Turnbull CG, Murfet IC, Beveridge CA. Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol 2001, 126(3):1205-1213.
37. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O. MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 2004, 14(14):1232-1238.
38. Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ. The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 2005, 17(3):746-759.
39. Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 2010, 61(2):300-311.
40. Ledger SE, Janssen BJ, Karunairetnam S, Wang T, Snowden KC. Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis). New Phytol 2010, 188(3):803-813.
41. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Nogue F, Rameau C. Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 2011, 138(8):1531-1539.
42. Kepinski S, Leyser O. Plant development: an axis of auxin. Nature 2003, 426(6963):132-135.
43. Leyser O. Regulation of shoot branching by auxin. Trends Plant Sci 2003, 8(11):541-545.
44. Auldridge ME, McCarty DR, Klee HJ. Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 2006, 9(3):315-321.
45. Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ. Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 2006, 45(6):982-993.
46. Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S. Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 2010, 51(7):1118-1126.
47. Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P. A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 2010, 6(10):741-749.
48. Cheng X, Ruyter-Spira C, Bouwmeester H. The interaction between strigolactones and other plant hormones in the regulation of plant development. Front Plant Sci 2013, 4:199.
49. Vallabhaneni R, Bradbury LM, Wurtzel ET. The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys 2010, 504(1):104-111.
50. Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA. The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 2005, 17(2):464-474.
51. Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 2007, 51(6):1019-1029.
52. Djennane S, Hibrand-Saint Oyant L, Kawamura K, Lalanne D, Laffaire M, Thouroude T, Chalain S, Sakr S, Boumaza R, Foucher F, Leduc N. Impacts of light and temperature on shoot branching gradient and expression of strigolactone synthesis and signalling genes in rose. Plant Cell Environ 2013, 37(3):742-757.
53. Liang YS, Jeon YA, Lim SH, Kim JK, Lee JY, Kim YM, Lee YH, Ha SH. Vascular-specific activity of the Arabidopsis carotenoid cleavage dioxygenase 7 gene promoter. Plant Cell Rep 2011, 30(6):973-980.
54. Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L. The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 2006, 48(5):687-698.
55. Drummond RS, Martinez-Sanchez NM, Janssen BJ, Templeton KR, Simons JL, Quinn BD, Karunairetnam S, Snowden KC. Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE7 is involved in the production of negative and positive branching signals in petunia. Plant Physiol 2009, 151(4):1867-1877.
56. Thimann KV, Skoog F. Studies on the Growth Hormone of Plants: III The Inhibiting Action of the Growth Substance on Bud Development. Proc Natl Acad Sci U S A 1933, 19(7):714-716.
57. Domagalska MA, Leyser O. Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 2011, 12(4):211-221.
58. Franklin KA. Light and temperature signal crosstalk in plant development. Curr Opin Plant Biol 2009, 12(1):63-68.
59. Kebrom TH, Burson BL, Finlayson SA. Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol 2006, 140(3):1109-1117.
60. Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ. Phytochrome regulation of branching in Arabidopsis. Plant Physiol 2010, 152(4):1914-1927.
61. Arumingtyas E, Floyd R, Gregory M, Murfet I. Branching in Pisum: inheritance and allelism tests with 17 ramosus mutants. Pisum Genet 1992, 24:14.
62. Beveridge CA, Ross JJ, Murfet IC. Branching in Pea (Action of Genes Rms3 and Rms4). Plant Physiol 1996, 110(3):859-865.
63. Sussex IM, Kerk NM. The evolution of plant architecture. Curr Opin Plant Biol 2001, 4(1):33-37.
64. Wasternack C, Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Botany 2013, 111(6):37.
65. Zhong W, Gao Z, Zhuang W, Shi T, Zhang Z, Ni Z. Genome-wide expression profiles of seasonal bud dormancy at four critical stages in Japanese apricot. Plant Mol Biol 2013, 83(3):247-264.
66. Qin Q, Kaas Q, Zhang C, Zhou L, Luo X, Zhou M, Sun X, Zhang L, Paek K-Y, Cui Y. The cold awakening of doritaenopsis 'tinny Tender' orchid flowers: the role of leaves in cold-induced Bud dormancy release. J Plant Growth Regul 2012, 31(2):139-155.
67. Sun J, Chen Q, Qi L, Jiang H, Li S, Xu Y, Liu F, Zhou W, Pan J, Li X, Palme K, Li C. Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol 2011, 191(2):360-375.
68. Wang J, Yan DW, Yuan TT, Gao X, Lu YT. A gain-of-function mutation in IAA8 alters Arabidopsis floral organ development by change of jasmonic acid level. Plant Mol Biol 2013, 82(1-2):71-83.
69. Muller D, Leyser O. Auxin, cytokinin and the control of shoot branching. Ann Bot 2011, 107(7):1203-1212.
70. Hartung W, Sauter A, Hose E. Abscisic acid in the xylem: where does it come from, where does it go to?. J Exp Bot 2002, 53(366):27-32.
71. Sakakibara H, Takei K, Hirose N. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 2006, 11(9):440-448.
72. Shimizu-Sato S, Tanaka M, Mori H. Auxin-cytokinin interactions in the control of shoot branching. Plant Mol Biol 2009, 69(4):429-435.
73. Esmaeili N, Ebrahimzadeh H, Abdi K, Safarian S. Determination of some phenolic compounds in Crocus sativus L. corms and its antioxidant activities study. Pharmacogn Mag 2011, 7(25):74-80.
74. Hayward A, Stirnberg P, Beveridge C, Leyser O. Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 2009, 151(1):400-412.
75. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH. Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 2003, 6(4):358-364.
76. Li CJ, Bangerth F. Autoinhibition of indoleacetic acid transport in the shoots of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiol Plant 1999, 106:5.
77. Dun EA, Brewer PB, Beveridge CA. Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci 2009, 14(7):364-372.
78. 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.
79. Napoli CA, Beveridge CA, Snowden KC. Reevaluating concepts of apical dominance and the control of axillary bud outgrowth. Curr Top Dev Biol 1999, 44:127-169.
80. Foo E, Turnbull CG, Beveridge CA. Long-distance signaling and the control of branching in the rms1 mutant of pea. Plant Physiol 2001, 126(1):203-209.
81. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 2011, 155(2):974-987.
82. Pasare SA, Ducreux LJ, Morris WL, Campbell R, Sharma SK, Roumeliotis E, Kohlen W, van der Krol S, Bramley PM, Roberts AG, Fraser PD, Taylor MA. The role of the potato (Solanum tuberosum) CCD8 gene in stolon and tuber development. New Phytol 2013, 198(4):1108-1120.
83. Johnson X, Brcich T, Dun EA, Goussot M, Haurogne K, Beveridge CA, Rameau C. Branching genes are conserved across species Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 2006, 142(3):1014-1026.
84. Thimann KV. Fifty years of plant hormone research. Plant Physiol 1974, 54(4):450-453.
85. Gocal GF, Pharis RP, Yeung EC, Pearce D. Changes after Decapitation in Concentrations of Indole-3-Acetic Acid and Abscisic Acid in the Larger Axillary Bud of Phaseolus vulgaris L. cv Tender Green. Plant Physiol 1991, 95(2):344-350.
86. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci U S A 2011, 108(50):20242-20247.
87. Walter MH, Floss DS, Strack D. Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 2010, 232(1):1-17.
88. Floss DS, Walter MH. Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited. Plant Signal Behav 2009, 4(3):172-175.
89. Ilg A, Yu Q, Schaub P, Beyer P, Al-Babili S. Overexpression of the rice carotenoid cleavage dioxygenase 1 gene in Golden Rice endosperm suggests apocarotenoids as substrates in planta. Planta 2010, 232(3):691-699.
90. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y. DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 2009, 21(5):1512-1525.
91. Grilli-Caiola M. Saffron reproductive biology. Acta Horticult 2004, 650:12.
92. Rubio A, Rambla JL, Santaella M, Gomez MD, Orzaez D, Granell A, Gomez-Gomez L. Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release. J Biol Chem 2008, 283(36):24816-24825.
93. Stark D. Anatomical and physiological studies of floral tube elongation of Crocus vernus iridaceae. Am J Bot 1982, 69(9):1476-1482.
94. Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 2008, 178(4):863-874.