Journal of Plant Research

, Volume 129, Issue 2, pp 241–250 | Cite as

Isolation, expression and evolution of FERTILIZATION INDEPENDENT ENDOSPERM homologs in Podostemaceae

  • Priyanka Khanduri
  • Roopam Sharma
  • Vishnu Bhat
  • Rajesh Tandon
Regular Paper
First Online:
Received:
Accepted:
  • 457 Downloads

Abstract

Podostemaceae is an interesting family of angiosperms with unusual development and morphology. Among these, double fertilization, a defining feature of angiosperms is invariably missing in the family. Consequently, embryo development in the seeds takes place without endosperm. In recent years, the role of polycomb genes has garnered much interest because of their crucial role in seed development. Some of these genes have been reported from many unrelated species, underlining their high conservation. Thus, it becomes exciting to know the role of these genes in podostemads, which are devoid of double fertilization and endosperm. Here, we report the isolation, characterization and expression patterns of homologs of Fertilization Independent Endosperm (FIE) in two species of Podostemaceae, Zeylanidium olivaceum and Polypleurum stylosum. FIE like homologs could be identified in Z. olivaceum (ZoFIE) and P. stylosum (PsFIE). The predicted amino acid sequence of FIE homologs showed similarity to other homologs, containing the conserved seven WD40 repeats. Expression studies revealed that ZoFIE and PsFIE transcripts were present in the vegetative tissue (thallus in Podostemaceae) and the seedlings, similar to the model plants. However, the ZoFIE and PsFIE expression disappeared in the flowering stages. This unique pattern of expression suggests that in the absence of double fertilization and endosperm the expression of FIS complex genes perhaps is obliterated in Podostemaceae.

Keywords

Aquatic angiosperm Fertilization Independent Endosperm Homologs Podostemaceae 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

PK is thankful to the Council of Scientific and Industrial Research for the award of Senior Research Fellowship. Financial assistance from the DU-R&D and DU/DST-PURSE Grant schemes is gratefully acknowledged. Thanks are due to the Forest Department, Kerala, India, for providing permission to collect the plant material and extending help during the field visits.

Supplementary material

10265_2015_771_MOESM1_ESM.pdf (3.3 mb)
Supplementary material 1 (PDF 3382 kb)
10265_2015_771_MOESM2_ESM.pdf (112 kb)
Supplementary material 2 (PDF 112 kb)

References

  1. Arekal GD, Nagendran CR (1975) Is there a Podostemum type of embryo sac in the genus Farmeria? Caryologia 28:229–235CrossRefGoogle Scholar
  2. Batygina TB, Bragina EA, Vasilyeva VE (2003) The reproductive system and germination in orchids. Acta Biol Cracov Bot 45:21–23Google Scholar
  3. Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou JP, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7:e1002014PubMedCentralCrossRefPubMedGoogle Scholar
  4. Chaudhary AM, Luo M, Miller C, Craig S, Dennis ES, Peacock WJ (1997) Fertilization independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci 94:4223–4228CrossRefGoogle Scholar
  5. Chaudhary A, Khanduri P, Tandon R, Uniyal PL, Mohan Ram HY (2014) Central cell degeneration leads to three-celled female gametophyte in Zeylanidium lichenoides Engl. (Podostemaceae). S Afr J Bot 91:99–106CrossRefGoogle Scholar
  6. Cook CDK, Rutishauser R (2007) Podostemaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 9. Springer, Berlin, pp 305–344Google Scholar
  7. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105:16831–16836PubMedCentralCrossRefPubMedGoogle Scholar
  8. Feil R, Berger F (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23:192–199CrossRefPubMedGoogle Scholar
  9. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  10. Gendall AR, Levy YY, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535CrossRefPubMedGoogle Scholar
  11. Ghawana S, Paul A, Kumar H, Kumar A, Singh H, Bhardwaj PK, Rani A, Singh RS, Raizada J, Singh K, Kumar S (2011) An RNA isolation system for plant tissues rich in secondary metabolites. BMC Res Notes 4:1–5CrossRefGoogle Scholar
  12. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44–51CrossRefPubMedGoogle Scholar
  13. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280:446–450CrossRefPubMedGoogle Scholar
  14. Guitton AE, Berger F (2005) Loss-of-function of MULTICOPY SUPPRESSOR OF IRA 1 produces non-viable parthenogenetic embryos in Arabidopsis. Curr Biol 15:750–754CrossRefPubMedGoogle Scholar
  15. Hennig L, Derkacheva M (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25:414–423CrossRefPubMedGoogle Scholar
  16. Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158:35–43PubMedCentralCrossRefPubMedGoogle Scholar
  17. Huh JH, Bauer MJ, Hsieh T, Fischer R (2007) Endosperm gene imprinting and seed development. Curr Opin Genet Dev 17:480–485PubMedCentralCrossRefPubMedGoogle Scholar
  18. Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2002) Plant systematics: a phylogenetic approach. Sinauer Associates, USAGoogle Scholar
  19. Katayama N, Koi S, Kato M (2010) Expression of SHOOT MERISTEMLESS, WUSCHEL, and ASYMMETRIC LEAVES1 homologs in the shoots of Podostemaceae: implications for the evolution of novel shoot organogenesis. Plant Cell 22:2131–2140PubMedCentralCrossRefPubMedGoogle Scholar
  20. Katz A, Oliva Mosquna A, Hakim O, Ohad N (2004) FIE and CURLY LEAF Polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37:707–719CrossRefPubMedGoogle Scholar
  21. Kinoshita T, Harada JJ, Goldberg RB, Fischer RL (2001) Polycomb repression of flowering during early plant development. Proc Natl Acad Sci USA 98:14156–14161PubMedCentralCrossRefPubMedGoogle Scholar
  22. Köhler C, Villar CB (2008) Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18:236–243CrossRefPubMedGoogle Scholar
  23. Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22:4804–4814PubMedCentralCrossRefPubMedGoogle Scholar
  24. Koi S, Fujinami R, Kubo N, Tsukamoto I, Inagawa R, Imaichi R, Kato M (2006) Comparative anatomy of root meristem and root cap in some species of Podostemaceae and the evolution of root dorsiventrality. Am J Bot 93:682–692CrossRefPubMedGoogle Scholar
  25. Korf I, Fan Y, Strome S (1998) The Polycomb group in Caenorhabditis elegans and maternal control of germline development. Development 125:2469–2478PubMedGoogle Scholar
  26. Leroy O, Hennig L, Breuninger H, Laux T, Köhler C (2007) Polycomb group proteins function in the female gametophyte to determine seed development in plants. Development 134:3639–3648CrossRefPubMedGoogle Scholar
  27. Lomsadze A, Ter-Hovhannisyan V, Chernoff Y, Borodovsky M (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 33:6494–6506PubMedCentralCrossRefPubMedGoogle Scholar
  28. Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, Chaudhury AM (1999) Genes controlling fertilization independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:296–301PubMedCentralCrossRefPubMedGoogle Scholar
  29. Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury AM (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 97:10637–10642PubMedCentralCrossRefPubMedGoogle Scholar
  30. Luo M, Platten D, Chaudhury AM, Peacock WJ, Dennis ES (2009) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2:711–723CrossRefPubMedGoogle Scholar
  31. Mohan Ram HY, Sehgal A (2007) Podostemaceae—an evolutionary enigma. In: Proceedings of national seminar on evolutionary biology and biotechnology, zoological survey of India, pp 37–66Google Scholar
  32. Molitor A, Shen WH (2013) The Polycomb complex PRC1: composition and function in plants. J Genet Genomics 40:231–238CrossRefPubMedGoogle Scholar
  33. Mosquna A, Katz A, Decker EL, Rensing SA, Reski R, Ohad N (2009) Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136:2433–2444CrossRefPubMedGoogle Scholar
  34. Ng J, Hart CM, Morgan K, Simon JA (2000) A Drosophila ESC–E(Z) protein complex is distinct from other Polycomb group complexes and contains covalently modified ESC. Mol Cell Biol 20:3069–3078PubMedCentralCrossRefPubMedGoogle Scholar
  35. Nowack MK, Shirzadi R, Dissmeyer N, Dolf A, Endl E, Grini PE, Schnittger A (2007) Bypassing genomic imprinting allows seed development. Nature 447:312–315CrossRefPubMedGoogle Scholar
  36. Ohad N, Margossian L, Hsu YC, Williams C, Repetti P, Fischer RL (1996) A mutation that allows endosperm development without fertilization. Proc Natl Acad Sci USA 93:5319–5324PubMedCentralCrossRefPubMedGoogle Scholar
  37. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB, Fischer RL (1999) Mutations in FIE, a WD Polycomb group gene, allow endosperm development without fertilization. Plant Cell 11:407–416PubMedCentralCrossRefPubMedGoogle Scholar
  38. Pien S, Grossniklaus U (2007) Polycomb group and trithorax group proteins in Arabidopsis. Biochim Biophys Acta 1769:375–382CrossRefPubMedGoogle Scholar
  39. Rodrigues JCM, Tucker MR, Johnson SD, Hrmova M, Koltunow AMG (2008) Sexual and apomictic seed formation in Hieraciumrequires the plant polycomb-group gene FERTILIZATION INDEPENDENT ENDOSPERM. Plant Cell 20:2372–2386PubMedCentralCrossRefPubMedGoogle Scholar
  40. Saitou N, Nei M (1987) Theneighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  41. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Gen 37:501–506CrossRefGoogle Scholar
  42. Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8:9–22CrossRefPubMedGoogle Scholar
  43. Sehgal A, Khurana JP, Sethi Ara H, Jain M (2007) Organ identity of the thalloid plant body of Griffithella hookeriana and Polypleurum stylosum—Podostemoideae (Podostemaceae). Pl Syst Evol 267:93–104CrossRefGoogle Scholar
  44. Sehgal A, Khurana JP, Sethi M, Hussain A (2011) Occurrence of unique three celled megagametophyte and single fertilization in an aquatic angiosperm-Dalzellia zeylanica (Podostemaceae-Tristichoideae). Sex Plant Reprod 24:199–210CrossRefPubMedGoogle Scholar
  45. Sehgal A, Mann N, Mohan Ram HY (2014) Structural and developmental variability in the female gametophyte of Griffithella hookeriana, Polypleurum stylosum, and Zeylanidium lichenoides and its bearing on the occurrence of single fertilization in Podostemaceae. Plant Reprod 27:205–223CrossRefPubMedGoogle Scholar
  46. Spillane C, Schmid KJ, Laoueille-Duprat S, Pien S, EscobarRestrepo JM, Baroux C, Gagliardini V, Page DR, Wolfe KH, Grossniklaus U (2007) Positive Darwinian selection at the imprinted MEDEA locus in plants. Nature 448:349–352CrossRefPubMedGoogle Scholar
  47. Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164CrossRefPubMedGoogle Scholar
  48. Suzuki K, Kita Y, Kato M (2002) Comparative developmental anatomy of seedlings in nine species of Podostemaceae (subfamily Podostemoideae). Ann Bot 89:755–765PubMedCentralCrossRefPubMedGoogle Scholar
  49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729PubMedCentralCrossRefPubMedGoogle Scholar
  50. Terasaka O, Niitsu T, Tanaka R (1979) Single fertilization in Spiranthes sinesis. J Plant Res 92:59–67Google Scholar
  51. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralCrossRefPubMedGoogle Scholar
  52. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analyses tools. Nucleic Acids Res 25:4876–4882PubMedCentralCrossRefPubMedGoogle Scholar
  53. Ungru A, Nowack MK, Reymond M, Shirzadi R, Kumar M, Biewers S, Grini PE, Schnittger A (2008) Natural variation in the degree of autonomous endosperm formation reveals independence and constraints of embryo growth during seed development in Arabidopsis thaliana. Genetics 179:829–841PubMedCentralCrossRefPubMedGoogle Scholar
  54. Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115CrossRefGoogle Scholar
  55. van Nocker S, Ludwig P (2003) The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genom 4:50CrossRefGoogle Scholar
  56. Vidyashankari B, Mohan Ram HY (1987) In vitro germination and origin of thallus in Griffithella hookeriana (Podostemaceae). Aquat Bot 28:161–169CrossRefGoogle Scholar
  57. Williams JH, Friedman WE (2004) The four-celled female gametophyte of Illicium (Illiciaceae: Austrobaileyales): its implication for understanding the origin and early evolution of monocots, eudicots and eumagnolids. Am J Bot 91:332–351CrossRefPubMedGoogle Scholar
  58. Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103:14631–14636PubMedCentralCrossRefPubMedGoogle Scholar
  59. Yadegari R, Kinoshita T, Lotan O et al (2000) Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell 12:2367–2382PubMedCentralCrossRefPubMedGoogle Scholar
  60. Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T, Sung ZR, Takahashi S (2001) EMBRYONIC FLOWER2, a novel Polycomb group protein homologue, mediates shoot development and flowering in Arabidopsis. Plant Cell 13:2471–2481PubMedCentralCrossRefPubMedGoogle Scholar
  61. Zinger NV, Poddubnaya-Arnoldi VA, Petrovskaia-Baranova TP (1964) Evolution of female embryonal structures in compositae and orchids. Byulleten’ Glavnogo Botanicheskogo Sada Akademii nauk SSSR. 55:81–90Google Scholar
  62. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic, New York, pp 97–166Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  • Priyanka Khanduri
    • 1
  • Roopam Sharma
    • 2
  • Vishnu Bhat
    • 1
  • Rajesh Tandon
    • 1
  1. 1.Department of BotanyUniversity of DelhiDelhiIndia
  2. 2.Department of Plant SciencesUniversity of SaskatchewanSaskatoonCanada

Personalised recommendations