Alternate Bearing in Citrus: Changes in the Expression of Flowering Control Genes and in Global Gene Expression in ON- versus OFF-Crop Trees

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Shalom, Liron ^a   Samuels, Sivan ^a   Zur, Naftali ^a   Shlizerman, Lyudmila ^a   Zemach, Hanita ^a   Weissberg, Mira ^a   Ophir, Ron ^a   Blumwald, Eduardo ^b   Sadka, Avi ^a  

^a VOLCANI CENTER   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVONOID; MICRORNA; MICRORNA156; TREHALOSE; UNCLASSIFIED DRUG;

AGRICULTURAL PROCEDURES; ALTERNATE BEARING; ARTICLE; BUD; CARBOHYDRATE METABOLISM; CITRUS; CONTROLLED STUDY; CROP; FLOWERING; FRUIT SET; GENE; GENE EXPRESSION; GENE INDUCTION; GENETIC ANALYSIS; GENETIC ENGINEERING AND GENE TECHNOLOGY; GLOBAL GENE EXPRESSION; METABOLOMICS; NONHUMAN; PHOTOSYNTHESIS; PLANT METABOLISM; SEASON; SIGNAL TRANSDUCTION; SPL GENE;

BIOSYNTHETIC PATHWAYS; CITRUS; CLUSTER ANALYSIS; FLAVONOIDS; FLOWERS; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TREHALOSE;

EID: 84867416699     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046930     Document Type: Article

References (69)

1. Monselise SP, Goldschmidt EE, (1982) Alternate bearing in fruit trees. Hortic rev 4: 128-173.
2. Garcia-Luis A, Fornes F, Guardiola JL, (1995) Leaf Carbohydrates and Flower Formation in Citrus. J Amer Soc Horticul Sci 120: 222-227.
3. Martinez-Fuentes A, Mesejo C, Reig C, Agusti M, (2010) Timing of the inhibitory effect of fruit on return bloom of 'Valencia' sweet orange (Citrus sinensis (L.) Osbeck). J Sci Food Agric 90: 1936-1943.
4. Okuda H, Kihara T, Iwagaki I, (1996) Effects of fruit removal on photosynthesis, stomatal conductance and ABA level in the leaves of vegetative shoots in relation to flowering of satsuma mandarin [Citrus unshiu]. J Jpn Soc Hortic Sci 65 (1): 15-20.
5. Verreynne JS, Lovatt CJ, (2009) The Effect of Crop Load on Budbreak Influences Return Bloom in Alternate Bearing 'Pixie' Mandarin. J Amer Soc Horticul Science 134: 299-307.
6. Goldschmidt EE, (1999) Carbohydrate supply as a critical factor for citrus fruit development and productivity. Hortscience 34: 1020-1024.
7. Goldschmidt EE, Golomb A, (1982) The Carbohydrate Balance of Alternate-bearing Citrus Trees and the Significance of Reserves for Flowering and Fruiting. J Am Soc Hort Sci 107: 206-208.
8. Hilgeman RH, Dunlap JA, Sharpless GC, (1967) Effect of time of harvest of 'Valencia' oranges on leaf carbohydrate content and subsequent set of fruit. Proc Amer Soc Hort Sci 90: 111-116.
9. Jones WW, Embleton TW, Barnhart EL, Gree CB, (1974) Effect of time and amount of fruit thinning on leaf carbohydrate and fruit set in 'valencia' oranges. Hilgardia 42: 441-449.
10. Jones WW, Embleton TW, M.L S, Cree CB, (1970) Carbohydrates and fruiting of 'Valencia' orange trees. J Am Soc Hort Sci 95: 380-381.
11. Li CY, Weiss D, Goldschmidt EE, (2003) Effects of carbohydrate starvation on gene expression in citrus root. Planta 217: 11-20.
12. Li CY, Weiss D, Goldschmidt EE, (2003) Girdling affects carbohydrate-related gene expression in leaves, bark and roots of alternate-bearing citrus trees. Ann Bot 92: 137-143.
13. Monselise SP, Goldschmidt EE, (1981) Alternate bearing in citrus and ways of control. Proc Int Soc Citriculture 1: 239-242.
14. Garcia-Luis A, Fornes F, Sanz A, Guardiola JL, (1988) The regulation of flowering and fruit set in citrus: relationship with carbohydrate levels. Israel J Bot 37: 189-201.
15. Garcia-Luis A, Kanduser M, Guardiola JL, (1995) The Influence of Fruiting on the Bud Sprouting and Flower Induction Responses to Chilling in Citrus. J Hortic Sci 70: 817-825.
16. Goldschmidt EE, Aschkenazi N, Herzano Y, Schaffer AA, Monselise SP, (1985) A role for carbohydrate-levels in the control of flowering in citrus. Sci Horticul 26: 159-166.
17. Krajewski AJ, Rabe E, (1995) Citrus Flowering- a Critical-Evaluation. J Hortic Sci 70: 357-374.
18. Monerri C, Fortunato-Almeida A, Molina RV, Nebauer SG, Garcia-Luis A, et al. (2011) Relation of carbohydrate reserves with the forthcoming crop, flower formation and photosynthetic rate, in the alternate bearing 'Salustiana' sweet orange (Citrus sinensis L.). Sci Horticul 129: 71-78.
19. Yahata D, Oba Y, Kuwahara M, (1995) Changes in carbohydrate levels, alpha-amylase activity, indoleacetic acid and gibberellin-like substances in the summer shoots of wase satsuma mandarin trees grown indoors during flower-bud differentiation. J Jpn Soc Hortic Sci 64: 527-533.
20. Bower JP, Lovatt CJ, Cutting JGM, Blanke MM, (1990) Inertaction of plant growth regulator and carbohydrate in flowering and fruit set. Acta Horticul 275: 425-434.
21. Erner Y, Lovatt CJ, Goell A, (1993) Regulation of flowering for improvement yield and profit in citrus. BARD final report.
22. Talon M, Tadeo FR, Ben-Cheikh W, Gomez-Cadenas A, Mehouachi J, et al. (1997) Hormonal regulation of fruit set and abscission in citrus: classical concepts and new evidence. Acta Horticul 463: 209-217.
23. Chao CCT, Khuong T, Zheng YS, Lovatt CJ, (2011) Response of evergreen perennial tree crops to gibberellic acid is crop load-dependent. I: GA(3) increases the yield of commercially valuable 'Nules' Clementine Mandarin fruit only in the off-crop year of an alternate bearing orchard. Sci Horticult 130: 743-752.
24. Jones WW, Coggins CW, Embleton TW, (1976) Endogenous abscisic acid in relation to bud growth in alternate bearing 'Valencia' orange. Plant Physiol 58: 681-682.
25. Koshita Y, Takahara T, Ogata T, Goto A, (1999) Involvement of endogenous plant hormones (IAA, ABA, GAs) in leaves and flower bud formation of satsuma mandarin (Citrus unshiu Marc.). Sci Horticul 79: 185-194.
26. Okuda H, (2000) A comparison of IAA and ABA levels in leaves and roots of two citrus cultivars with different degrees of alternate bearing. J Hortic Sci Biotech 75: 355-359.
27. Goldschmidt EE, Tamim M, Goren R, (1997) Gibberellins and flowering in Citrus and other fruit trees: A critical analysis. Acta Horticult 463: 201-208.
28. Muñoz-Fambuena N, Mesejo C, González-Mas MC, Iglesias DJ, Primo-Millo E, et al. (2012) Gibberellic acid reduces flowering intensity in sweet orange [Citrus sinensis (L.) Osbeck] by repressing CiFT gene expression. J Plant Growth Regul Published online.
29. Guitton B, Kelner JJ, Velasco R, Gardiner SE, Chagne D, et al. (2012) Genetic control of biennial bearing in apple. J Experim Bot 63: 131-149.
30. Davenport TL, (1990) Citrus flowering. Horticul Rev 12: 349-408.
31. Lord EM, Eckard KJ, (1985) Shoot Development in Citrus-Sinensis L (Washington Navel Orange). 1. Floral and Inforescence Ontogeny. Bot Gazette 146: 320-326.
32. Lord EM, Eckard KJ, (1987) Shoot Development in Citrus-Sinensis L (Washington Navel Orange). 2. Alteration of Developmental Fate of Flowering Shoots after Ga3 Treatment. Bot Gazette 148: 17-22.
33. Monselise SP, (1985) Citrus and related genera. CRC Handbook of flowering 2: 275-294.
34. Tan FC, Swain SM, (2007) Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). Physiol Plant 131: 481-495.
35. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, et al. (2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Trans Res 14: 703-712.
36. Pêna L, Martin-Trillo M, Juarez J, Pina JA, Navarro L, et al. (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotech 19: 263-267.
37. Pillitteri LJ, Lovatt CJ, Walling LL, (2004) Isolation and characterization of LEAFY and APETALA1 homologues from Citrus sinensis L. Osbeck 'Washington'. J Am Soc Hort Sci 129: 846-856.
38. Nishikawa F, Endo T, Shimada T, Fujii H, Shimizu T, et al. (2007) Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). J Exper Bot 58: 3915-3927.
39. Pillitteri LJ, Lovatt CJ, Walling LL, (2004) Isolation and characterization of a TERMINAL FLOWER homolog and its correlation with juvenility in citrus. Plant Physiol 135: 1540-1551.
40. Muñoz-Fambuena N, Mesejo C, González-Mas MC, Primo-Millo E, Agustí M, et al. (2011) Fruit regulates seasonal expression of flowering genes in alternate bearing 'Moncada' mandarin. Ann Botany 108: 511-519.
41. Bain JM, (1958) Morphological and physiological changes in the development fruit of the Valencia orange. Aust J Bot 6: 1-25.
42. Ruzin SE, (1999) Plant Microtechnique and Microscopy. Oxford University Press, Cambridge.
43. Chang S, Puryear J, Cairney J, (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Repor 11: 113-116.
44. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, et al. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotech 26: 317-325.
45. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
46. Wettenhall JM, Smyth GK, (2004) limmaGUI: A graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706.
47. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, et al. (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant Cell Envir 32: 1211-1229.
48. Samach A, (2012) Congratulations, you have been carefully chosen to represent an important developmental regulator. Annals of Botany in press.
49. Wu G, Poethig RS, (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539-3547.
50. Fornara F, Coupland G, (2009) Plant Phase Transitions Make a SPLash. Cell 138: 625-627.
51. Duarte AMM, Garcia-Luis A, Molina RV, Monerri C, Navarro V, et al. (2006) Long-term effect of winter gibberellic acid sprays and auxin applications on crop value of 'Clausellina' satsuma. J Am Soc Horticul Sci 131: 586-592.
52. Guardiola JL, Arguelles T, (1977) Hormonal control of senescence in excised orange leaves. J Horticul Sci 52: 199-204.
53. Guardiola JL, Monerri C, Agusti M, (1982) The inhibitory effect of gibberellic acid on flowering in Citrus. Physiol Plant 55: 136-142.
54. Nakagawa M, Honsho C, Kanzaki S, Shimizu K, Utsunomiya N, (2012) Isolation and expression analysis of FLOWERING LOCUS T-like and gibberellin metabolism genes in biennial-bearing mango trees. Sci Horticul 139: 108-117.
55. Hanke MV, Flachowsky H, Peil A, Hattasch C, (2007) No flower no fruit- genetic potentials to trigger flowering in fruit trees. Genes Genomes Genomics 1: 1-20.
56. Kotoda N, Hayashi H, Suzuki M, Igarashi M, Hatsuyama Y, et al. (2010) Molecular Characterization of FLOWERING LOCUS T-Like Genes of Apple (Malusdomestica Borkh.). Plant Cell Physiol 51: 561-575.
57. Hsu CY, Adams JP, Kim HJ, No K, Ma CP, et al. (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 108: 10756-10761.
58. Corbesier L, Coupland G, (2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant Cell Envir 28: 54-66.
59. Henderson IR, Dean C, (2004) Control of Arabidopsis flowering: the chill before the bloom. Development 131: 3829-3838.
60. Searle I, He YH, Turck F, Vincent C, Fornara F, et al. (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes & Development 20: 898-912.
61. Wang JW, Park MY, Wang LJ, Koo YJ, Chen XY, et al. (2011) MiRNA Control of Vegetative Phase Change in Trees. Plos Genetics 7.
62. Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, et al. (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49: 683-693.
63. Wang JW, Czech B, Weigel D, (2009) miR156-Regulated SPL Transcription Factors Define an Endogenous Flowering Pathway in Arabidopsis thaliana. Cell 138: 738-749.
64. Ramon M, Rolland F, (2007) Plant development: introducing trehalose metabolism. Tren Plant Sci 12: 185-188.
65. Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, et al. (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136: 3649-3659.
66. van Dijken AJH, Schluepmann H, Smeekens SCM, (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135: 969-977.
67. Winkel-Shirley B, (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5: 218-223.
68. Grace SC, Logan BA, (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Phil Trans Royal Soc London, Series B-Biol Sci 355: 1499-1510.
69. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P, (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140: 637-646.