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Planta

, Volume 221, Issue 2, pp 222–230 | Cite as

Identification and fine mapping of a mutant gene for palealess spikelet in rice

  • Qiong Luo
  • Kaida Zhou
  • Xianfeng Zhao
  • Qianchun Zeng
  • Hongai Xia
  • Wenxue Zhai
  • Jichen Xu
  • Xianjun Wu
  • Hongsong Yang
  • Lihuang ZhuEmail author
Original Article

Abstract

In grass, the evolutionary relationship between lemma and palea, and their relationship to the flower organs in dicots have been variously interpreted and wildely debated. In the present study, we carried out morphological and genetic analysis of a palealess mutant (pal) from rice (Oryza sativa L.), and fine mapping the gene responsible for the mutated trait. Together, our findings indicate that the palea is replaced by two leaf-like structures in the pal flowers, and this trait is controlled by one recessive gene, termed palealess1 (pal1). With a large F2 segregating population, the pal1 gene was finally mapped into a physical region of 35 kb. Our results also suggest that the lemma and palea of rice are not homologous organs, palea is likely evolutionarily equivalent to the eudicot sepal, and the pal1 should be an A function gene for rice floral organ identity.

Keywords

Rice Floral organ identity Flower development Palealess mutant Finemapping 

Abbreviations

pal

Palealess mutant

pal1

Palealess1

PAL1

PALEALESS1

SEM

Scanning electron microscopy

EREBP

Ethylene-responsive element-binding protein

AP2-like

APETALA2-like

ap1-1

Apetala1-1

ap2-1

Apetala2-1

Notes

Acknowledgements

We would like to thank Prof. K.D. Zhou (Rice Research Institute of Sichuan Agriculture University, China) for providing parental materials, Dr X.Q. Wang (Institute of Genetics and Developmental Biology, CAS, China) for technical assistance in microscopy, and Prof. W. Xue (Institute of Biophysics, CAS, China) for SEM analysis. This work was supported by a grant from the National Natural Science Foundation of China (30370797).

References

  1. Akagi H, Yokozeki Y, Inagaki A, Nakamura A, Fujimura T (1996) A codominant DNA marker closely linked to the rice nuclear restorer gene, RF-1, identified with inter-SSR fingerprinting. Genome 39:1205–1209PubMedGoogle Scholar
  2. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579CrossRefPubMedGoogle Scholar
  3. Barry GF (2001) The use of the Monsanto draft rice genome sequence in research. Plant Physiol 125:1164–1165CrossRefPubMedGoogle Scholar
  4. Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489CrossRefPubMedGoogle Scholar
  5. Bell AD (1991) Plant form. Oxford University Press, New YorkGoogle Scholar
  6. Bowman JL (1997) Evolutionary conservation of angiosperm flower development at the molecular and genetic leves. J Biosci 22:515–527Google Scholar
  7. Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52CrossRefPubMedGoogle Scholar
  8. Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedGoogle Scholar
  9. Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72:85–95CrossRefPubMedGoogle Scholar
  10. Causse MA, Fulton TM, Cho YG, Ahn SN, Chunwongse J, Wu K, Xiao J, Yu Z, Ronald PC, Harrington SE et al (1994) Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138:1251–1274PubMedGoogle Scholar
  11. Chen X, Wu R (1997) Direct amplification of unknown genes and fragments by Uneven polymerase chain reaction. Gene 185:195–199CrossRefPubMedGoogle Scholar
  12. Chen X, Temnykh S, Xu Y, Cho YG, McCouch SR (1997) Development of microsatellite framework map providing genomewide coverage in rice (Oryza sativa L.). Theor Appl Genet 95:553–567CrossRefGoogle Scholar
  13. Chung YY, Kim SR, Finkel D, Yanofsky MF, An G (1994) Early flowering and reduced apical dominance result from ectopic expression of a rice MADS box gene. Plant Mol Biol 26:657–665CrossRefPubMedGoogle Scholar
  14. Clifford HT (1987) Spikelet and floral morphology. In: Soderstrom TR, Hilu KW, Campbell CS, Barkworth ME (eds) Grass systematics and evolution. Smithsonian Institution Press, Washington DC, pp 21–30Google Scholar
  15. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedGoogle Scholar
  16. Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7:1859–1868CrossRefPubMedGoogle Scholar
  17. Cook RJ (1998) Toward a successful multinational crop plant genome initiative. Proc Natl Acad Sci USA 95:1993–1995CrossRefPubMedGoogle Scholar
  18. Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the monocotyledons. Springer, BerlinGoogle Scholar
  19. Delseny M (2004) Re-evaluating the relevance of ancestral shared synteny as a tool for crop improvement. Curr Opin Plant Biol 7:126–131CrossRefPubMedGoogle Scholar
  20. Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002CrossRefPubMedGoogle Scholar
  21. Eckardt NA (2000) Sequencing the rice genome. Plant Cell 12:2011–2017CrossRefPubMedGoogle Scholar
  22. Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, Jia P, Zhao Q, Ying K, Yu S, Tang Y, Weng Q, Zhang L, Lu Y, Mu J, Zhang LS, Yu Z, Fan D, Liu X, Lu T, Li C, Wu Y, Sun T, Lei H, Li T, Hu H, Guan J, Wu M, Zhang R, Zhou B, Chen Z, Chen L, Jin Z, Wang R, Yin H, Cai Z, Ren S, Lv G, Gu W, Zhu G, Tu Y, Jia J, Chen J, Kang H, Chen X, Shao C, Sun Y, Hu Q, Zhang X, Zhang W, Wang L, Ding C, Sheng H, Gu J, Chen S, Ni L, Zhu F, Chen W, Lan L, Lai Y, Cheng Z, Gu M, Jiang J, Li J, Hong G, Xue Y, Han B (2002) Sequence and analysis of rice chromosome 4. Nature 420:316–320CrossRefPubMedGoogle Scholar
  23. Ferrario S, Immink RG, Angenent GC (2004) Conservation and diversity in flower land. Curr Opin Plant Biol 7:84–91CrossRefPubMedGoogle Scholar
  24. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100CrossRefPubMedGoogle Scholar
  25. Goodman HM, Ecker JR, Dean C (1995) The genome of Arabidopsis thaliana. Proc Natl Acad Sci USA 92:10831–10835PubMedGoogle Scholar
  26. Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Genet Dev 11:449–456CrossRefPubMedGoogle Scholar
  27. Greco R, Stagi L, Colombo L, Angenent GC, Sari-Gorla M, Pe ME (1997) MADS box genes expressed in developing inflorescences of rice and sorghum. Mol Gen Genet 253:615–623CrossRefPubMedGoogle Scholar
  28. Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2:741–753CrossRefPubMedGoogle Scholar
  29. Jeon JS, Jang S, Lee S, Nam J, Kim C, Lee SH, Chung YY, Kim SR, Lee YH, Cho YG, An G (2000) leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12:871–884CrossRefPubMedGoogle Scholar
  30. Kang HG, Jeon JS, Lee S, An G (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 38:1021–1029CrossRefPubMedGoogle Scholar
  31. Keck E, McSteen P, Carpenter R, Coen E (2003) Separation of genetic functions controlling organ identity in flowers. Embo J 22:1058–1066CrossRefPubMedGoogle Scholar
  32. Komatsu M, Chujo A, Nagato Y, Shimamoto K, Kyozuka J (2003) FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets. Development 130:3841–3850CrossRefPubMedGoogle Scholar
  33. Kyozuka J, Kobayashi T, Morita M, Shimamoto K (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes. Plant Cell Physiol 41:710–718PubMedGoogle Scholar
  34. Lander ES, Green P, Abrahamson J (1987) MAPMARKER:an interactive computer for constructing primary genetics linkage maps of experimental and natural populations. Genetics 1:174–181Google Scholar
  35. Lohmann JU, Weigel D (2002) Building beauty: the genetic control of floral patterning. Dev Cell 2:135–142CrossRefPubMedGoogle Scholar
  36. Lopez-Dee ZP, Wittich P, Enrico Pe M, Rigola D, Del Buono I, Gorla MS, Kater MM, Colombo L (1999) OsMADS13, a novel rice MADS-box gene expressed during ovule development. Dev Genet 25:237–244CrossRefPubMedGoogle Scholar
  37. Ma H, dePamphilis C (2000) The ABCs of floral evolution. Cell 101:5–8CrossRefPubMedGoogle Scholar
  38. McCouch SR, Kochert G, Yu ZH, Wang ZY, Khush GS, Coffman WR, Tanksley SD (1988) Molecular mapping of rice chromosomes. Theor Appl Genet 76:815–820Google Scholar
  39. Meas T, Van de Steene N, Van Montagu M, Gerats T (1998) AP2-like genes of Petunia hybrida. flowering newsl 25:35–40Google Scholar
  40. Moon YH, Jung JY, Kang HG, An G (1999) Identification of a rice APETALA3 homologue by yeast twohybrid screening. Plant Mol Biol 40:167–177CrossRefPubMedGoogle Scholar
  41. Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130:705–718CrossRefPubMedGoogle Scholar
  42. Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195CrossRefPubMedGoogle Scholar
  43. Pozzi C, Faccioli P, Terzi V, Stanca AM, Cerioli S, Castiglioni P, Fink R, Capone R, Muller KJ, Bossinger G, Rohde W, Salamini F (2000) Genetics of mutations affecting the development of a barley floral bract. Genetics 154:1335–1346PubMedGoogle Scholar
  44. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedGoogle Scholar
  45. Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y, Antonio BA, Kanamori H, Hosokawa S, Masukawa M, Arikawa K, Chiden Y, Hayashi M, Okamoto M, Ando T, Aoki H, Arita K, Hamada M, Harada C, Hijishita S, Honda M, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, Ito S, Ito T, Ito Y, Iwabuchi A, Kamiya K, Karasawa W, Katagiri S, Kikuta A, Kobayashi N, Kono I, Machita K, Maehara T, Mizuno H, Mizubayashi T, Mukai Y, Nagasaki H, Nakashima M, Nakama Y, Nakamichi Y, Nakamura M, Namiki N, Negishi M, Ohta I, Ono N, Saji S, Sakai K, Shibata M, Shimokawa T, Shomura A, Song J, Takazaki Y, Terasawa K, Tsuji K, Waki K, Yamagata H, Yamane H, Yoshiki S, Yoshihara R, Yukawa K, Zhong H, Iwama H, Endo T, Ito H, Hahn JH, Kim HI, Eun MY, Yano M, Jiang J, Gojobori T (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316CrossRefPubMedGoogle Scholar
  46. Shinozuka Y, Kojima S, Shomura A, Ichimura H, Yano M, Yamamoto K, Sasaki T (1999) Isolation and characterization of rice MADS box gene homologues and their RFLP mapping. DNA Res 6:123–129PubMedGoogle Scholar
  47. Takeoka Y, Shimizu M, Wada T (1993) Panicles. In: Hoshikawa TMaH (ed) Science of the rice plant, vol I. Nobunkyo, Tokyo, pp 295–326Google Scholar
  48. Theissen G (2000) Plant biology. Shattering developments. Nature 404:711–713CrossRefPubMedGoogle Scholar
  49. Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85CrossRefPubMedGoogle Scholar
  50. Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471CrossRefPubMedGoogle Scholar
  51. Theissen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516PubMedGoogle Scholar
  52. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149CrossRefPubMedGoogle Scholar
  53. Trobner W, Ramirez L, Motte P, Hue I, Huijser P, Lonnig WE, Saedler H, Sommer H, Schwarz-Sommer Z (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. Embo J 11:4693–4704PubMedGoogle Scholar
  54. Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205PubMedGoogle Scholar
  55. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509CrossRefPubMedGoogle Scholar
  56. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Li J, Liu Z, Qi Q, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Zhao W, Li P, Chen W, Zhang Y, Hu J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Tao M, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Qiong Luo
    • 1
  • Kaida Zhou
    • 2
  • Xianfeng Zhao
    • 1
  • Qianchun Zeng
    • 3
  • Hongai Xia
    • 1
  • Wenxue Zhai
    • 1
  • Jichen Xu
    • 1
  • Xianjun Wu
    • 2
  • Hongsong Yang
    • 2
  • Lihuang Zhu
    • 1
    Email author
  1. 1.Institute of Genetics and Developmental BiologyChinese Academy of ScienceBeijingChina
  2. 2.Rice Research Institute of Sichuan Agriculture UniversityWenjiangChina
  3. 3.Faculty of Agronomy and BiotechnologyYunnan Agricultural UniversityKunmingChina

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