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Genetica

, Volume 147, Issue 2, pp 121–130 | Cite as

TaEPFL1, an EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) secreted peptide gene, is required for stamen development in wheat

  • Qingxu Sun
  • Jipeng Qu
  • Yan Yu
  • Zaijun YangEmail author
  • Shuhong Wei
  • Yilei Wu
  • Jun Yang
  • Zhengsong Peng
Review

Abstract

Members of the EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) family play diverse roles in plant growth and development, including the guidance of inflorescence architecture and pedicel length. In this work, we identified and characterized the EFPL gene TaEPFL1 from the wheat pistillody mutant HTS-1. Sequence alignment and phylogenetic analysis indicated that TaEPFL1 belongs to the EPFL1 gene. Quantitative real-time RT-PCR analysis showed that the TaEPFL1 gene is expressed at an abnormally high level in pistillody stamens compared with that in pistils and stamens. Heterologous expression of the TaEPFL1 gene in Arabidopsis caused shortened filaments and pedicels and might reduce the level of AtACO2 gene expression. These results suggest that TaEPFL1 plays an important role in the development of stamen and that overexpression of TaEPFL1 results in abnormal stamens. We deduced that the overexpression of the TaEPFL1 gene may contribute to the homeotic transformation of stamens into pistils or pistil-like structures in wheat. These data offer insights into the molecular mechanism of pistillody mutation in wheat.

Keywords

Wheat TaEPFL1 gene Pistillody mutant Overexpression Stamen development 

Abbreviations

EPFL

EPIDERMAL PATTERNING FACTOR-LIKE

HTS-1

Homologous transformation sterility-1

Col-0

Arabidopsis thaliana ecotype Columbia

ACO

1-Aminocyclopropane-1-carboxylate oxidase

ACS

1-Aminocyclopropane-1-carboxylate synthase

SAM

S-Adenosyl-l-methionine synthase

Notes

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant number 31760425), Foundation of Science and Technology department of Sichuan Province, China (Grant number 16JC022), National General Cultivation Project of China West Normal University (Grant number 17C043), and the Innovation Team Project of Education Department of Sichuan Province (Grant number 16TD0020).

Compliance with ethical standards

Conflict of interest

All authors declare that they no conflict of interest.

References

  1. Abrash EB, Bergmann DC (2010) Regional specification of stomatal production by the putative ligand CHALLAH. Development 137:447–455CrossRefGoogle Scholar
  2. Abrash EB, Davies KA, Bergmann DC (2011) Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand–receptor interactions. Plant Cell 23:2864–2879CrossRefGoogle Scholar
  3. Balague C, Walson CF, Turner AJ, Rouge P, Picton S, Pech JC, Grierson D (1993) Isolation of a ripening and wound- induced cDNA from Cucumis melo L. encoding a protein with homology to the ethylene forming enzyme. Eur J Biochem 212:27–34CrossRefGoogle Scholar
  4. Barrett CH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3(4):274–284CrossRefGoogle Scholar
  5. Belderok B, Mesdag H, Donner DA (2000) Bread-making quality of wheat. Kluwer Academic Publishers, AmsterdamCrossRefGoogle Scholar
  6. Besshouehara K, Wang DR, Furuta T, Minami A, Nagai K, Gamuyao R et al (2016) Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. Proc Natl Acad Sci USA 113:8969–8974CrossRefGoogle Scholar
  7. Chen YH, Fu XM, Wu H, Zang J (2012) CsACO4, an ACC oxidase gene regulating male differentiation in cucumber. Afr J Biotechnol 11(67):13069–13074CrossRefGoogle Scholar
  8. Duan QH, Wang DH, Xu ZH and Bai SN (2008) Stamen development in Arabidopsis is arrested by organ-specific overexpression of a cucumber ethylene synthesis gene CsACO2. Planta 228(4):537–543CrossRefGoogle Scholar
  9. Hama E, Takumi S, Ogihara Y, Murai K (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218:712–720CrossRefGoogle Scholar
  10. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031CrossRefGoogle Scholar
  11. Huang Y, Tao ZS, Liu Q, Wang XF, Yu JY, Liu GH, Wang HZ (2014) BnEPFL6, an EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) secreted peptide gene, is required for filament elongation in Brassica napus. Plant Mol Biol 85:505–517CrossRefGoogle Scholar
  12. Hunt L, Bailey KJ, Gray JE (2010) The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol 186:609–614CrossRefGoogle Scholar
  13. Jewaria PK, Hara T, Tanaka H, Kondo T, Betsuyaku S, Sawa S, Sakagami Y, Aimoto S, Kakimoto T (2013) Differential effect of peptides stomagen, EPF1 and EPF2 on activation of MAP kinase MPK6 and SPCH protein level. Plant Cell Physiol 54:1253–1262CrossRefGoogle Scholar
  14. Jin J et al (2016) GAD1 encodes a secreted peptide that regulates grain number, grain length and awn development in rice domestication. Plant Cell 28(10):2453–2463CrossRefGoogle Scholar
  15. Knopf RR, Trebitsh T (2006) The female-specific Cs-ACS1G gene of cucumber. A case of gene duplication and recombination between the non-sex-specific 1-aminocyclopropane-1-carboxylate synthase gene and a branched-chain amino acid transaminase gene. Plant Cell Physiol 47(9):1217–1228CrossRefGoogle Scholar
  16. Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, Mizuno S, Masuda Y, Irie K, Tanaka Y, Takada S, Kakimoto T, Sakagami Y (2010) Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol 51:1–8CrossRefGoogle Scholar
  17. Kosentka PZ, Overholt A, Maradiaga R, Mitoubsi O, Shpak ED (2019) EPFL signals in the boundary region of the SAM restrict its size and promote leaf initiation. Plant Physiol 179:265–279CrossRefGoogle Scholar
  18. Laubinger S, Zeller G, Henz SR, Sachsenberg T, Widmer CK, Naouar N, Vuylsteke M, Scholkopf B, Ratsch G, Weigel D (2008) At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol 9(7):R112CrossRefGoogle Scholar
  19. 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 25:402–408CrossRefGoogle Scholar
  20. Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J Exp Bot 62:1677–1686CrossRefGoogle Scholar
  21. Murai K, Takumi S, Koga H, Ogihara Y (2002) Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear–cytoplasm interaction in wheat. Plant J 29:169–181CrossRefGoogle Scholar
  22. Murai K, Miyamae M, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44:1255–1265CrossRefGoogle Scholar
  23. Peng ZS, Yang ZJ, Ouyang ZM, Yang H (2013) Characterization of a novel pistillody mutant in common wheat. Aust J Crop Sci 7:159–164Google Scholar
  24. Rudich J (1969) Increase in femaleness of three cucurbits by treatment with Ethrel, an ethylene-releasing compound. Planta 86:69–76CrossRefGoogle Scholar
  25. Shewry PR (2009) Wheat. J Exp Bot 60(6):1537–1553CrossRefGoogle Scholar
  26. Steven JC, Andrew FB (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743CrossRefGoogle Scholar
  27. Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–244CrossRefGoogle Scholar
  28. Takatsuji H, Nakamura N, Katsumoto Y (1994) A new family of zinc finger proteins in petunia: structure, DNA sequence recognition, and floral organ-specific expression. Plant Cell 6:947–958CrossRefGoogle Scholar
  29. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefGoogle Scholar
  30. Tsao TH (1988) Sex expression in flowering. Acta Phytophysiol Sin 14:203–207Google Scholar
  31. Uchida N, Tasaka M (2013) Regulation of plant vascular stem cells by endodermis-derived EPFL-family peptide hormones and phloem-expressed ERECTA-family receptor kinases. J Exp Bot 64(17):5335–5343CrossRefGoogle Scholar
  32. Uchida N, Lee JS, Horst RJ, Lai HH, Kajita R, Kakimoto T, Tasaka M, Torii KU (2012) Regulation of inflorescence architecture by intertissue layer ligand–receptor communication between endodermis and phloem. Proc Natl Acad Sci USA 109(16):6337–6342CrossRefGoogle Scholar
  33. Yamada K, Saraike T, Shitsukawa N, Hirabayashi C, Takumi S, Murai K (2009) Class D and B sister MADS-box genes are associated with ectopic ovule formation in the pistil-like stamens of alloplasmic wheat (Triticum aestivum L.). Plant Mol Biol 71:1–14CrossRefGoogle Scholar
  34. Yang ZJ, Peng ZS, Yang H, Yang J, Wei SH, Cai P (2011) Suppression subtractive hybridization identified differentially expressed genes in pistil mutations in wheat. Plant Mol Bio Rep 29:431–439CrossRefGoogle Scholar
  35. Yang ZJ, Peng ZS, Wei SH, Liao ML, Yu Y, Jang ZY (2015) Pistillody mutant reveals key insights into stamen and pistil development in wheat (Triticum aestivum L.). BMC Genom 16:211–220CrossRefGoogle Scholar
  36. Yang Q, Yang ZJ, Tang HF, Yu Y, Chen ZY, Wei SH, Sun QX, Peng ZS (2018) High-density genetic map construction and mapping of the homologous transformation sterility gene (hts) in wheat using GBS markers. BMC Plant Biol 18:301CrossRefGoogle Scholar
  37. Yin T, Quinn JA (1992) A mechanistic model of a single hormone regulating both sexes in flowering plants. Bull Torrey Bot Club 119:431–441CrossRefGoogle Scholar
  38. Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26:1579–1597CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Qingxu Sun
    • 1
  • Jipeng Qu
    • 2
  • Yan Yu
    • 1
  • Zaijun Yang
    • 1
    Email author
  • Shuhong Wei
    • 1
  • Yilei Wu
    • 1
  • Jun Yang
    • 1
  • Zhengsong Peng
    • 2
  1. 1.Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), College of Life ScienceChina West Normal UniversityNanchongPeople’s Republic of China
  2. 2.School of Agricultural ScienceXichang UniversityXichangPeople’s Republic of China

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