Early steps of adventitious rooting: Morphology, hormonal profiling and carbohydrate turnover in carnation stem cuttings

Physiologia Plantarum

Volumn 150, Issue 3, 2014, Pages 446-462

  Agulló Antón, María Ángeles ^a   Ferrández Ayela, Almudena ^b   Fernández García, Nieves ^c   Nicolás, Carlos ^d   Albacete, Alfonso ^c   Pérez Alfocea, Francisco ^c   Sánchez Bravo, José ^a   Pérez Pérez, José Manuel ^b   Acosta, Manuel ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^c RESEARCH GROUP ON QUALITY   (Spain)

^d UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DIANTHUS CARYOPHYLLUS;

1 AMINOCYCLOPROPANECARBOXYLIC ACID; 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID; 6 N (3,3 DIMETHYLALLYL)ADENOSINE; ABSCISIC ACID; AMINO ACID; CYTOKININ; DRUG DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; PHYTOHORMONE; SALICYLIC ACID DERIVATIVE; VEGETABLE PROTEIN; ZEATIN RIBOSIDE;

ARTICLE; CARBOHYDRATE METABOLISM; CARNATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT ROOT; PLANT STEM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TISSUE CULTURE TECHNIQUE; ULTRASTRUCTURE;

ABSCISIC ACID; AMINO ACIDS, CYCLIC; CARBOHYDRATE METABOLISM; CYTOKININS; DIANTHUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; ISOPENTENYLADENOSINE; MICROSCOPY, ELECTRON, SCANNING; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALICYLATES; TISSUE CULTURE TECHNIQUES;

EID: 84893802931     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/ppl.12114     Document Type: Article

References (83)

1. Abu-Abied M, Szwerdszarf D, Mordehaev I, Levy A, Stelmakh OR, Belausov E, Yaniv Y, Uliel S, Katzenellenbogen M, Riov J, Ophir R, Sadot E (2013) Microarray analysis revealed upregulation of nitrate reductase in juvenile cuttings of Eucalyptus grandis, which correlated with increased nitric oxide production and adventitious root formation. Plant J 71: 787-799
2. Acosta M, Oliveros-Valenzuela MR, Nicolas C, Sanchez-Bravo J (2009) Rooting of carnation cuttings. The auxin signal. Plant Signal Behav 4: 234-236
3. Agulló-Antón MA, Olmos E, Perez-Perez JM, Acosta M (2013) Evaluation of ploidy level and endoreduplication in carnation (Dianthus spp.). Plant Sci 201-202: 1-11
4. Agulló-Antón MA, Sánchez Bravo J, Acosta M, Druege U (2011) Auxins or sugars: what makes the difference in the adventitious rooting of stored carnation cuttings? J Plant Growth Regul 30: 100-113
5. Ahkami AH, Lischewski S, Haensch KT, Porfirova S, Hofmann J, Rolletschek H, Melzer M, Franken P, Hause B, Druege U, Hajirezaei MR (2009) Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol 181: 613-625
6. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109-120
7. Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59: 4119-4131
8. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53: 2039-2055
9. Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56: 1535-1544
10. Balibrea M, Cuartero J, Bolarín MC, Pérez-Alfocea F (2003) Sucrolytic activities during fruit development of Lycopersicon genotypes differing in tolerance to salinity. Physiol Plant 118: 38-46
11. Balibrea M, Santa Cruz AM, Bolarín MC, Pérez-Alfocea F (1996) Sucrolytic activities in relation to sink strength and carbohydrate composition in tomato fruit growing under salinity. Plant Sci 118: 47-55
12. Benkova E, Ivanchenko MG, Friml J, Shishkova S, Dubrovsky J (2009) A morphogenetic trigger: is there an emerging concept in plant developmental biology? Trends Plant Sci 14: 189-193
13. Bergmeyer HU, Bernt E (1974) Sucrose. In: Bergmeyer HU (ed) Methods of Enzymatic Analysis. Academic Press, New York, pp 1176-1179
14. Blakesley D (1994) Auxin metabolism and adventitious root initiation. In: Davis TD, Haissig BE (eds) Biology of Adventitious Root Formation. Plenum Press, New York, pp 143-154
15. Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Onckelen HV, Van Montagu M, Inzé D (1995) superroot a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7: 1405-1419
16. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
17. Brinker M, van Zyl L, Liu W, Craig D, Sederoff RR, Clapham DH, von Arnold S (2004) Microarray analyses of gene expression during adventitious root development in Pinus contorta. Plant Physiol 135: 1526-1539
18. Caño-Delgado A, Lee JY, Demura T (2010) Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu Rev Cell Dev Biol 26: 605-637
19. Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121: 53-60
20. Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, Cheng Y, Zhao Y, Xie Q, Zhang XS (2013) Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3. Plant Physiol 161: 24-251
21. Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661-677
22. Chickarmane VS, Gordon SP, Tarr PT, Heisler MG, Meyerowitz EM (2012) Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc Natl Acad Sci USA 109: 4002-4007
23. de Klerk GJ, Hanecakova J, Jasik J (2001) The role of cytokinins in rooting of stem slices cut from apple microcuttings. Plant Biosyst 135: 79-84
24. de Klerk GJ, Van der Krieken W, de Jong JC (1999) Review. The formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Dev Biol Plant 35: 189-199
25. Delessert C, Wilson IW, Van Der Straeten D, Dennis ES, Dolferus R (2004) Spatial and temporal analysis of the local response to wounding in Arabidopsis leaves. Plant Mol Biol 55: 165-181
26. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86: 423-433
27. Dodd IC (2005) Root-to-shoot signalling: assessing the roles of 'up' in the up and down world of long-distance signalling in planta. Plant Soil 274: 251-270
28. Doehlert DC, Felker FC (1987) Characterization and distribution of invertase activity in developing maize (Zea mays) kernels. Physiol Plant 70: 51-57
29. Eklöf S, Astot C, Sitbon F, Moritz T, Olsson O, Sandberg G (2000) Transgenic tobacco plants co-expressing Agrobacterium iaa and ipt genes have wild-type hormone levels but display both auxin- and cytokinin-overproducing phenotypes. Plant J 23: 279-284
30. Fernández-García N, Carvajal M, Olmos E (2004) Graft union formation in tomato plants: peroxidase and catalase involvement. Ann Bot 93: 53-60
31. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449: 1053-1057
32. Garrido G, Cano EA, Arnao MB, Acosta M, Sánchez-Bravo J (1996) Influence of cold storage period and auxin treatment on the subsequent rooting of carnation cuttings. Sci Hortic 65: 73-84
33. Garrido G, Cano EA, Acosta M, Sánchez-Bravo J (1998) Formation and growth of roots in carnation cuttings: influence of cold storage period and auxin treatment. Sci Hortic 74: 219-231
34. Garrido G, Guerrero JR, Cano EA, Acosta M, Sánchez-Bravo J (2002) Origin and basipetal transport of the IAA responsible for rooting of carnation cuttings. Physiol Plant 114: 303-312
35. Geiss G, Gutierrez L, Bellini C (2009) Adventitious root formation: new insights and perspectives. In: Beeckman T (ed) Annual Plant Reviews Volume 37: Root Development. Wiley-Blackwell, Oxford, UK, pp 127-156
36. Gómez-Cadenas A, Tadeo FR, Primo-Millo E, Talon M (1998) Involvement of abscisic acid and ethylene in the responses of citrus seedlings to salt shock. Physiol Plant 103: 475-484
37. Guerrero JR, Garrido G, Acosta M, Sánchez-Bravo J (1999) Influence of 2, 3, 5-triiodobenzoic acid and 1-N-naphthylphthalamic acid on indoleacetic acid transport in carnation cuttings: relationship with rooting. J Plant Growth Regul 18: 183-190
38. Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21: 3119-3132
39. Gutierrez L, Mongelard G, Flokova K, Pacurar DI, Novak O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24: 2515-2527
40. Hause B, Hause G, Kutter C, Miersch O, Wasternack C (2003) Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol 44: 643-648
41. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Van Montagu M, Inzé D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proc Natl Acad Sci USA 101: 5146-5151
42. Hwang I, Sakakibara H (2006) Cytokinin biosynthesis and perception. Physiol Plant 126: 528-538
43. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15: 1560-1565
44. Klopotek Y, Haensch KT, Hause B, Hajirezaei MR, Druege U (2010) Dark exposure of petunia cuttings strongly improves adventitious root formation and enhances carbohydrate availability during rooting in the light. J Plant Physiol 167: 547-554
45. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7: 235-246
46. Konieczny R, Kepczynski J, Pilarska M, Cembrowska D, Menzel D, Samaj J (2009) Cytokinin and ethylene affect auxin transport-dependent rhizogenesis in hypocotyls of common ice plant (Mesembryanthemum crystallinum L.). J Plant Growth Regul 28: 331-340
47. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10: 249
48. Kuroha T, Kato H, Asami T, Yoshida S, Kamada H, Satoh S (2002) A trans-zeatin riboside in root xylem sap negatively regulates adventitious root formation on cucumber hypocotyls. J Exp Bot 53: 2193-2200
49. Kwon HK, Wang MH (2011) The D-type cyclin gene (Nicta;CycD3;4) controls cell cycle progression in response to sugar availability in tobacco. J Plant Physiol 168: 133-139
50. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Maree AF, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6: e307
51. León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52: 1-9
52. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25: 402-408
53. Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002-1004
54. Mergemann H, Sauter M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124: 609-614
55. Meuwly P, Molders W, Buchala A, Metraux JP (1995) Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiol 109: 1107-1114
56. Naija S, Elloumi N, Jbir N, Ammar S, Kevers C (2008) Anatomical and biochemical changes during adventitious rooting of apple rootstocks MM 106 cultured in vitro. C R Biol 331: 518-525
57. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61: 3-15
58. Nordstrom AC, Jacobs FA, Eliasson L (1991) Effect of exogenous indole-3-acetic acid and indole-3-butyric acid on internal levels of the respective auxins and their conjugation with aspartic acid during adventitious root formation in pea cuttings. Plant Physiol 96: 856-861
59. Normanly J, Bartel B (1999) Redundancy as a way of life-IAA metabolism. Curr Opin Plant Biol 2: 207-213
60. O'Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274: 1914-1917
61. Oliveros-Valenzuela MR, Reyes D, Sánchez-Bravo J, Acosta M, Nicolas C (2008) Isolation and characterization of a cDNA clone encoding an auxin influx carrier in carnation cuttings. Expression in different organs and cultivars and its relationship with cold storage. Plant Physiol Biochem 46: 1071-1076
62. Pelleschi S, Rocher JP, Prioul JL (1997) Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell Environ 20: 493-503
63. Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14: 399-408
64. Pop TI, Pamfil D, Bellini C (2011) Auxin control in the formation of adventitious roots. Not Bot Horti Agrobo 39: 309-316
65. Ramírez-Carvajal GA, Morse AM, Dervinis C, Davis JM (2009) The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol 150: 759-771
66. Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge CA (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158: 1976-1987
67. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9: 606-613
68. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57: 431-449
69. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814
70. Sheela VL (2008) Carnation. In: Sheela VL, Sheela MN (eds) Flowers for Trade. New India Publishing, New Delhi, pp 95-112
71. Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11: 118-130
72. Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, McKhann H, Garcion C, Vaucheret H, Sandberg G, Bellini C (2005) Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17: 1343-1359
73. Swarup R, Peret B (2012) AUX/LAX family of auxin influx carriers-an overview. Front Plant Sci 3: 225
74. Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45: 1028-1036
75. van Berkel K, de Boer RJ, Scheres B, ten Tusscher K (2013) Polar auxin transport: models and mechanisms. Development 140: 2253-2268
76. Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63: 551-562
77. Visser E, Cohen JD, Barendse G, Blom C, Voesenek L (1996) An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol 112: 1687-1692
78. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100: 681-697
79. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532-2550
80. Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46: 1674-1681
81. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15: 1566-1571
82. Zeevaart JAD (1980) Changes in the levels of abscisic acid and its metabolites in excised leaf blades of Xanthium strumarium during and after water stress. Plant Physiol 66: 672-678
83. Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145: 450-464