Theoretical and Applied Genetics

, Volume 126, Issue 5, pp 1273–1283 | Cite as

Structure, transcription and post-transcriptional regulation of the bread wheat orthologs of the barley cleistogamy gene Cly1

  • Shunzong Ning
  • Ning Wang
  • Shun Sakuma
  • Mohammad Pourkheirandish
  • Jianzhong Wu
  • Takashi Matsumoto
  • Takato Koba
  • Takao Komatsuda
Original Paper

Abstract

The majority of genes present in the hexaploid bread wheat genome are present as three homoeologs. Here, we describe the three homoeologous orthologs of the barley cleistogamy gene Cly1, a member of the AP2 gene family. As in barley, the wheat genes (designated TaAP2-A, -B and -D) map to the sub-telomeric region of the long arms of the group 2 chromosomes. The structure and pattern of transcription of the TaAP2 homoeologs were similar to those of Cly1. Transcript abundance was high in the florets, and particularly in the lodicule. The TaAP2 message was cleaved at its miR172 target sites. The set of homoeolog-specific PCR assays developed will be informative for identifying either naturally occurring or induced cleistogamous alleles at each of the three wheat homoeologs. By combining such alleles via conventional crossing, it should be possible to generate a cleistogamous form of bread wheat, which would be advantageous both with respect to improving the level of the crop’s resistance against the causative pathogen of fusarium head blight, and for controlling pollen-mediated gene flow to and from genetically modified cultivars.

Supplementary material

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References

  1. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741PubMedCrossRefGoogle Scholar
  2. Ban T, Suenaga K (2000) Genetic analysis of resistance to fusarium head blight caused by Fusarium graminearum in Chinese wheat cultivar Sumai 3 and the Japanese cultivar Saikai 165. Euphytica 113:87–99CrossRefGoogle Scholar
  3. Bartel DP (2009) MicroRNAs: Target recognition and regulatory functions. Cell 136:215–233PubMedCrossRefGoogle Scholar
  4. Bottley A, Xia GM, Koebner RMD (2006) Homoeologous gene silencing in hexaploid wheat. Plant J 47:897–906PubMedCrossRefGoogle Scholar
  5. Brown RH, Bregitzer P (2011) A Ds insertional mutant of a barley mir172 gene results in indeterminate spikelet development. Crop Sci 51:1664–1672CrossRefGoogle Scholar
  6. Chapman V, Miller TE, Riley R (1976) Equivalence of the a genome of bread wheat and that of Triticum urartu. Genet Res 27:69–76CrossRefGoogle Scholar
  7. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025PubMedCrossRefGoogle Scholar
  8. Chhabra AK, Sethi SK (1991) Inheritance of cleistogamic flowering in durum wheat (Triticum durum). Euphytica 55:147–150CrossRefGoogle Scholar
  9. Chuck G, Meeley R, Irish E, Sakai H, Hake S (2007) The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 39:1517–1521PubMedCrossRefGoogle Scholar
  10. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  11. Comai L, Tyagi AP, Winter K, Holmes-Davis R, Reynolds SH, Stevens Y, Byers B (2000) Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12:1551–1567PubMedGoogle Scholar
  12. De Vries AP (1971) Flowering biology of wheat, particularly in view of hybrid seed production—a review. Euphytica 20:152–170CrossRefGoogle Scholar
  13. Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307CrossRefGoogle Scholar
  14. Fu YB, Somers DJ (2009) Genome-wide reduction of genetic diversity in wheat breeding. Crop Sci 49:161–168CrossRefGoogle Scholar
  15. Gilsinger J, Kong L, Shen X, Ohm H (2005) DNA markers associated with low fusarium head blight incidence and narrow flower opening in wheat. Theor Appl Genet 110:1218–1225PubMedCrossRefGoogle Scholar
  16. Glover B (2007) Understanding flowers and flowering. New York, Oxford, p 227CrossRefGoogle Scholar
  17. Henikoff S, Till BJ, Comai L (2004) TILLING. Traditional mutagenesis meets functional genomics. Plant Physiol 135:630–636PubMedCrossRefGoogle Scholar
  18. Heslop-Harrison Y, Heslop-Harrison JS (1996) Lodicule function and filament extension in the grasses: potassium ion movement and tissue specialization. Ann Bot 77:573–582CrossRefGoogle Scholar
  19. Hori K, Kobayashi T, Sato K, Takeda T (2005) QTL analysis of fusarium head blight resistance using a high-density linkage map in barley. Theor Appl Genet 111:1661–1672PubMedCrossRefGoogle Scholar
  20. Ishikawa G, Nakamura T, Ashida T, Saito M, Nasuda S, Endo TR, Wu J, Matsumoto T (2009) Localization of anchor loci representing five hundred annotated rice genes to wheat chromosomes using PLUG markers. Theor Appl Genet 118:499–514PubMedCrossRefGoogle Scholar
  21. Jofuku KD, den Boer BG, Montagu MV, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225PubMedGoogle Scholar
  22. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217PubMedCrossRefGoogle Scholar
  23. Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agric Hortic 19:889–890Google Scholar
  24. Kilian B, Özkan H, Deusch O, Effgen S, Brandolini A, Kohl J, Martin W, Salamini F (2007) Independent wheat B and G genome origins in outcrossing Aegilops progenitor haplotypes. Mol Biol Evol 24:217–227PubMedCrossRefGoogle Scholar
  25. Kirby EJM, Appleyard M (1981) Cereal development guide. National Agricultural center Cereal Unit, Stoneleigh, Warwickshire, UKGoogle Scholar
  26. Komatsuda T, Nakamura I, Takaiwa F, Oka S (1998) Development of STS markers closely linked to the vrs1 locus in barley, Hordeum vulgare. Genome 41:680–685Google Scholar
  27. Kubo K, Kawada N, Fujita M, Hatta K, Oda S, Nakajima T (2010) Effect of cleistogamy on fusarium head blight resistance in wheat. Breeding Sci 60:405–411CrossRefGoogle Scholar
  28. Ma R, Zheng DS, Fan L (1996) The crossability percentages of 96 bread wheat landraces and cultivars from Japan with rye. Euphytica 92:301–330Google Scholar
  29. Matus- Cádiz MA, Hucl P, Dupuis B (2007) Pollen-mediated gene flow in wheat at the commercial scale. Crop Sci 47:573–579CrossRefGoogle Scholar
  30. McMullen M, Jones R, Gallenberg D (1997) Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 81:1340–1348CrossRefGoogle Scholar
  31. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, Dulay GP, Hua KL, Ankoudinova I, Cost GJ, Urnov FD, Zhang HS, Holmes MC, Zhang L, Gregory PD, Rebar EJ (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143–148PubMedCrossRefGoogle Scholar
  32. Nair SK, Wang N, Turuspekov Y, Pourkheirandish M, Sinsuwongwat S, Chen G, Sameri M, Tagiri A, Honda I, Watanabe Y, Kanamori H, Wicker T, Stein N, Nagamura Y, Matsumoto T, Komatsuda T (2010) Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. Proc Natl Acad Sci USA 107:490–495PubMedCrossRefGoogle Scholar
  33. Nevo E (2009) Ecological genomics of natural plant populations: the Israeli perspective. In: Somers DJ, Langridge P, Gustafson JP (eds) Methods in molecular biology, plant genomics, vol 513. Human Press, A part of Springer Science + Business Media, pp 321–344Google Scholar
  34. Nevo E (2011) Triticum. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, cereals. Springer, Berlin, pp 407–456CrossRefGoogle Scholar
  35. Parry DW, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small grain cereals. Plant Pathol 44:207–238CrossRefGoogle Scholar
  36. Petersen G, Seberg O, Yde M, Berthelsen K (2006) Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum). Mol Phylogenet Evol 39:70–82PubMedCrossRefGoogle Scholar
  37. Riley R, Unrau J, Chapman V (1958) Evidence on the origin of the B genome of wheat. J Hered 49:91–98Google Scholar
  38. Sato K, Hori K, Takeda K (2008) Detection of fusarium head blight resistance QTLs using five populations of top-cross progeny derived from two-row × two-row crosses in barley. Mol Breeding 22:517–526CrossRefGoogle Scholar
  39. Sears ER (1954) The aneuploids of common wheat. Univ Mo Agric Exp Stn Bull 572:1–58Google Scholar
  40. Sears ER (1966) Nullisomic-tetrasomic combinations in hexaploid wheat. In: Rilly R, Lewis KR (eds) Chromosome manipulations and plant genetics. Oliver and Boyd, Edinburgh, pp 29–45Google Scholar
  41. Sears ER, Sears MS (1978) The telocentric chromosomes of commonwheat. In: Ramanujam S (ed) Proceedings of the 5th international wheat genetics symposium. Indian Society of Genetics and Plant Breeding, New Delhi, pp 389–407Google Scholar
  42. Sethi K, Chhabra AK (1990) Cleistogamy in wheat. Rachis 9:34–36Google Scholar
  43. Shitsukawa N, Tahira C, Kassai KI, Hirabayashi C, Shimizu T, Takumi S, Mochida K, Kawaura K, Ogihara Y, Murai Y (2007) Genetic and epigenetic alteration among three homoeologous genes of a class E MADS box gene in hexaploid wheat. Plant Cell 19:1723–1737PubMedCrossRefGoogle Scholar
  44. Simons KJ, Fellers JP, Trick HN, Zhang ZC, Tai YS, Gill BS (2006) Molecular characterization of the major wheat domestication gene Q. Genetics 172:547–555PubMedCrossRefGoogle Scholar
  45. Snijders CHA (1990) Fusarium head blight and mycotoxin contamination of wheat, a review. Eur J Plant Pathol 96:187–198Google Scholar
  46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  47. Tang M, Li G, Chen M (2007) The phylogeny and expression pattern of APETALA2-like genes in rice. J Genet Genomics 34:930–938PubMedCrossRefGoogle Scholar
  48. Theissen G, Saedler H (2001) Floral quartets. Nature 409:469–471PubMedCrossRefGoogle Scholar
  49. Turuspekov Y, Mano Y, Honda I, Kawada N, Watanabe Y, Komatsuda T (2004) Identification and mapping of cleistogamy genes in barley. Theor Appl Genet 109:480–487PubMedCrossRefGoogle Scholar
  50. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD (2010) Genome editing with engineered zinc finger nucleases. Nat Rev Genet 11:636–646PubMedCrossRefGoogle Scholar
  51. Wood AJ, Lo TW, Zeitler B, Pickle CS, Ralston EJ, Lee AH, Amora R, Miller JC, Leung E, Meng X, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Meyer BJ (2011) Targeted genome editing across species using ZFNs and TALENs. Science 333:307PubMedCrossRefGoogle Scholar
  52. Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J, Fujii F, Shomura A, Ando T, Kono I, Waki K, Yamamoto K, Yano M, Matsumoto T, Sasaki T (2002) A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14:525–535PubMedCrossRefGoogle Scholar
  53. Zhang Z, Belcram H, Gornicki P, Charles M, Just J, Huneau C, Magdelenat G, Couloux A, Samain S, Gill BS, Rasmussen JB, Barbe V, Faris JD, Chalhoub B (2011) Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proc Natl Acad Sci USA 108:18737–18742PubMedCrossRefGoogle Scholar
  54. Zhou Y, Lu D, Li C, Luo J, Zhu BF, Zhu J, Shangguan Y, Wang Z, Sang T, Zhou B, Han B (2012) Genetic Control of Seed Shattering in Rice by the APETALA2 Transcription Factor SHATTERING ABORTION1. Plant Cell 24:1034–1048PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Shunzong Ning
    • 1
    • 2
  • Ning Wang
    • 1
  • Shun Sakuma
    • 1
    • 2
  • Mohammad Pourkheirandish
    • 1
  • Jianzhong Wu
    • 1
  • Takashi Matsumoto
    • 1
  • Takato Koba
    • 2
  • Takao Komatsuda
    • 1
  1. 1.Plant Genome Research UnitNational Institute of Agrobiological Sciences (NIAS)TsukubaJapan
  2. 2.Graduate school of HorticultureChiba UniversityMatsudoJapan

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