Functional analysis of B and C class floral organ genes in spinach demonstrates their role in sexual dimorphism

BMC Plant Biology

Volumn 10, Issue , 2010, Pages

  Sather, D Noah ^a,b   Jovanovic, Maja ^a   Golenberg, Edward M ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNOLIOPHYTA; SPINACIA OLERACEA;

MESSENGER RNA; VEGETABLE PROTEIN;

ALLELE; ANTIBODY SPECIFICITY; ARTICLE; BIOLOGICAL MODEL; FERTILITY; FLOWER; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFORMATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR EVOLUTION; PLANT GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT; SPINACH; TISSUE FIXATION;

ALLELES; EVOLUTION, MOLECULAR; FERTILITY; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; IN SITU HYBRIDIZATION; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; PLANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX CHARACTERISTICS; SPINACIA OLERACEA; TISSUE FIXATION; TRANSFORMATION, GENETIC;

EID: 77949442411     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-10-46     Document Type: Article

References (59)

1. He C, Munster T, Saedler H. On the origin of floral morphological novelties. FEBS Lett 2004, 567(1):147-151. 10.1016/j.febslet.2004.02.090, 15165908.
2. Kanno A, Nakada M, Akita Y, Hirai M. Class B gene expression and the modified ABC model in nongrass monocots. ScientificWorldJournal 2007, 7:268-279. 10.1100/tsw.2007.86, 17334618.
3. Kanno A, Saeki H, Kameya T, Saedler H, Theissen G. Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Molecular Biology 2003, 52(4):831-841. 10.1023/A:1025070827979, 13677470.
4. Hirai M, Kamimura T, Kanno A. The expression patterns of three class B genes in two distinctive whorls of petaloid tepals in Alstroemeria ligtu. Plant Cell Physiol 2007, 48(2):310-321. 10.1093/pcp/pcm004, 17205968.
5. Park JH, Ishikawa Y, Ochiai T, Kanno A, Kameya T. Two GLOBOSA-like genes are expressed in second and third whorls of homochlamydeous flowers in Asparagus officinalis L. Plant Cell Physiol 2004, 45(3):325-332. 10.1093/pcp/pch040, 15047881.
6. Irish VF, Kramer EM. Genetic and molecular analysis of angiosperm flower development. Advances in Botanical Research 1998, 28:197-230.
7. He C, Saedler H. Hormonal control of the inflated calyx syndrome, a morphological novelty, in Physalis. Plant J 2007, 49(5):935-946. 10.1111/j.1365-313X.2006.03008.x, 17316177.
8. He C, Saedler H. Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proc Natl Acad Sci USA 2005, 102(16):5779-5784. 10.1073/pnas.0501877102, 556287, 15824316.
9. Kramer EM, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago PM. Elaboration of B Gene Function to Include the Identity of Novel Floral Organs in the Lower Eudicot Aquilegia. Plant Cell 2007, 19(3):750-766. 10.1105/tpc.107.050385, 1867376, 17400892.
10. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky M, Schmidt RJ. Molecular and genetic analysis of the Silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 2000, 5:569-579. 10.1016/S1097-2765(00)80450-5, 10882141.
11. Kyozuka J, Kobayashi T, Morita M, Shimamoto K. Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol 2000, 41:710-718.
12. Munster T, Ursula Wingen L, Faigl W, Werth S, Saedler H, Thei[ss]en G. Characterization of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses. Gene 2001, 262(1-2):1-13. 10.1016/S0378-1119(00)00556-4, 11179662.
13. Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ. Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 2004, 131(24):6083-6091. 10.1242/dev.01523, 15537689.
14. Xiao H, Wang Y, Liu D, Wang W, Li X, Zhao X, Xu J, Zhai W, Zhu L. Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference. Plant Molecular Biology 2003, 52:957-966. 10.1023/A:1025401611354, 14558657.
15. Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. Embo J 1999, 18(14):4023-4034. 10.1093/emboj/18.14.4023, 1171478, 10406807.
16. Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano H-Y. Functional Diversification of the Two C-Class MADS Box Genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 2006, 18(1):15-28. 10.1105/tpc.105.037200, 1323481, 16326928.
17. Heslop-Harrison J. Sex expression in flowering plants. Brookhaven Symposia in Biology 1964, 16:109-125. Upton, NY.: Brookhaven National Laboratory.
18. Golenberg EM, Freeman DC. Environmental sex expression, sexual lability, biased sex ratios and other X-rated stories from the far-red side of the garden. Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues 2006, 280-291. Japan: Global Science Books, Silva JATd.
19. Delong A, Calderon-Urrea A, Dellaporta S. Sex-determination gene Tasselseed2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 1993, 74:757-768. 10.1016/0092-8674(93)90522-R, 8358795.
20. Ainsworth C, Crossley S, Buchanan Wollaston V, Thangavelu M, Parker J. Male and female flowers of the dioecious plant sorrel show different patterns of MADS box gene expression. Plant Cell 1995, 7(10):1583-1598. 10.1105/tpc.7.10.1583, 161015, 7580253.
21. Kater M, Franken J, Carney K, Colombo L, Angenent G. Sex determination in the monoecious species cucumber is confined to specific floral whorls. Plant Cell 2001, 13:481-493. 10.1105/tpc.13.3.481, 135508, 11251091.
22. Hardenack S, Ye D, Saedler H, Grant S. Comparison of MADS box gene expression in developing male and female flowers of the dioecious plant White Campion. Plant Cell 1994, 6:1775-1787. 10.1105/tpc.6.12.1775, 160561, 7866023.
23. Hobza R, Hrusakova P, Safar J, Bartos J, Janousek B, Zluvova J, Michu E, Dolezel J, Vyskot B. MK17, a specific marker closely linked to the gynoecium suppression region on the Y chromosome in Silene latifolia. Theor Appl Genet 2006, 113(2):280-287. 10.1007/s00122-006-0293-3, 16791694.
24. Zluvova J, Nicolas M, Berger A, Negrutiu I, Moneger F. Premature arrest of the male flower meristem precedes sexual dimorphism in the dioecious plant Silene latifolia. Proc Natl Acad Sci USA 2006, 103(49):18854-18859. 10.1073/pnas.0606622103, 1693751, 17132741.
25. Di Stilio VS, Kramer EM, Baum DA. Floral MADS box genes and homeotic gender dimorphism in Thalictrum dioicum (Ranunculaceae) - a new model for the study of dioecy. Plant J 2005, 41(5):755-766. 10.1111/j.1365-313X.2005.02336.x, 15703062.
26. Pfent C, Pobursky KJ, Sather DN, Golenberg EM. Characterization of SpAPETALA3 and SpPISTILLATA, B Class Floral Identity Genes in Spinacia oleracea, and Their Relationship to Sexual Dimorphism. Development Genes and Evolution 2005, 215:132-142. 10.1007/s00427-004-0459-4, 15660251.
27. Sather DN, York A, Pobursky KJ, Golenberg EM. Sequence evolution and sex-specific expression patterns of the C class floral identity gene, SpAGAMOUS, in dioecious Spinacia oleracea L. Planta 2005, 222:284-292. 10.1007/s00425-005-1544-2, 15940462.
28. Sherry RA, Eckard KJ, Lord EM. Flower development in dioecious Spinacia oleracea (Chenopodiaceae). American Journal of Botany 1993, 80:283-291.
29. Golenberg EM, Sather DN, Hancock LC, Buckley KJ, Villafranco NM, Bisaro DM. Development of a gene silencing DNA vector derived from a broad host range geminivirus. Plant Methods 2009, 5(1):9. 10.1186/1746-4811-5-9, 2713212, 19573239.
30. Goto K, Meyerowitz EM. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes and Development 1994, 8(13):1548-1560. 10.1101/gad.8.13.1548, 7958839.
31. Devon RS, Porteous DJ, Brookes AJ. Splinkerettes--improved vectorettes for greater efficiency in PCR walking. Nucl Acids Res 1995, 23(9):1644-1645. 10.1093/nar/23.9.1644, 306912, 7784225.
32. Hill TA, Day CD, Zondlo SC, Thackeray AG, Irish VF. Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 1998, 125:1711-1721.
33. Folter S, Angenent GC. trans meets cis in MADS science. Trends in Plant Science 2006, 11(5):224-231. 10.1016/j.tplants.2006.03.008, 16616581.
34. Lamb RS, Hill TA, Tan QK-G, Irish VF. Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 2002, 129(9):2079-2086.
35. Busch MA, Bomblies K, Weigel D. Activation of a floral homeotic gene in Arabidopsis. Science 1999, 285(5427):585-587. 10.1126/science.285.5427.585, 10417388.
36. Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell 1993, 5(7):729-737. 10.1105/tpc.5.7.729, 160311, 8103379.
37. Ainsworth C, Rahman A, Parker J, Edwards G. Intersex inflorescences of Rumex acetosa demonstrate that sex determination is unique to each flower. New Phytol 2005, 165(3):711-720. 10.1111/j.1469-8137.2005.01281.x, 15720682.
38. Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 2004, 430(6997):356-360. 10.1038/nature02733, 15254538.
39. Bowman JL, Smyth DR, Meyerowitz EM. Genetic interactions among floral homeotic genes of Arabidopsis. Development 1991, 112:1-20.
40. Sather D, Golenberg E. Duplication of AP1 within the Spinacia oleracea L. AP1/FUL clade is followed by rapid amino acid and regulatory evolution. Planta 2009, 229(3):507-521. 10.1007/s00425-008-0851-9, 19005675.
41. Riechmann JL, Krizek BA, Meyerowitz EM. Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 1996, 93:4793-4798. 10.1073/pnas.93.10.4793, 39358, 8643482.
42. Riechmann JL, Meyerowitz EM. Determination of floral organ identity by Arabidopsis MADS domain homeotic proteins AP1, AP3, PI, and AG is independent of their DNA-binding specificity. Mol Biol Cell 1997, 8:1243-1259. 276150, 9243505.
43. Riechmann JL, Wang M, Meyerowitz EM. DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res 1996, 24(16):3134-3141. 10.1093/nar/24.16.3134, 146081, 8774892.
44. Honma T, Goto K. The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 2000, 127:2021-2030.
45. Schwarz-Sommer Z, Hue I, Huijser P, Flor P, Hansen R, Tetens F, Lonnig W, Saedler H, Sommer H. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J 1992, 11(1):251-263. 556446, 1346760.
46. Freeman DC, Vitale JJ. The influence of environment on the sex ratio and fitness of spinach. Botanical Gazette 1985, 146:137-142.
47. Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM. Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 2004, 101(20):7827-7832. 10.1073/pnas.0402377101, 419691, 15128937.
48. Chailakhyan MK. Genetic and hormonal regulation of growth, flowering, and sex expression in plants. American Journal of Botany 1979, 66:717-736.
49. Pobursky KJ. Early flower development and the influence of gibberellic acid on sex expression in Spinacia oleracea. Master of Science 2000, Detroit, MI: Wayne State University.
50. Charlesworth B, Charlesworth D. A model for the evolution of the dioecy and gynodioecy. Am Nat 1978, 112:975-997.
51. Rosa JT. Sex expression in spinach. Hilgardia 1925, 1:259-274.
52. Janick J, Stevenson EC. A genetic study of the heterogametic nature of the staminate plant in spinach. Proc Am Soc Hort Sci 1954, 63:444-446.
53. Janick J, Mahoney DL, Pfahler PL. The trisomics of Spinacia oleracea L. Journal of Heredity 1959, 50:46-50.
54. Mahoney DL, Janick J, Stevenson EC. Sex determination in diploid-triploid crosses of Spinacia oleracea. American Journal of Botany 1959, 46:372-375.
55. Ellis JR, Janick J. The chromosomes of Spinacia oleracea. American Journal of Botany 1960, 47:210-214.
56. Iizuka M, Janick J. Sex chromosome variation in Spinacia oleracea L. J Heredity 1971, 62:349-352.
57. Ramanna MS. Are there heteromorphic sex chromosomes in spinach (Spinacia oleracea L.)?. Euphytica 1976, 25:277-284.
58. Khattak J, Torp A, Andersen S. A genetic linkage map of Spinacia oleracea and localization of a sex determination locus. Euphytica 2006, 148(3):311-318.
59. Chailakhyan MK, Khrianin VN. Sexuality in plants and its hormonal regulation. 1987, New York: Springer-Verlag.