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Functional genomics of microspore embryogenesis

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Abstract

Isolated plant microspores, when stressed and cultured in vitro, can be diverted from their normal gametophytic pathway towards sporophytic development, with the formation of haploid embryos and ultimately doubled-haploid plants. This process is called androgenesis or microspore embryogenesis, and is widely used in plant breeding programmes to generate homozygous lines for breeding purposes. Protocols for the induction of microspore embryogenesis and the subsequent regeneration of doubled haploid (DH) plants have been successfully developed for more than 200 species. These practical advances stand in stark contrast to our knowledge of the underlying molecular genetic mechanism controlling this process. The majority of information regarding the genetic and molecular control of the developmental switch from gametophytic to sporophytic development has been garnered from four intensely studied (crop) plants comprising two dicotyledonous species, rapeseed (Brassica napus) and tobacco (Nicotiana tabacum), and two monocotyledonous species, wheat (Triticum aestivum) and barley (Hordeum vulgare). In these species the efficiency of microspore embryogenesis is very high and reproducible, making them suitable models for molecular studies. In the past, molecular studies on microspore embryogenesis have focussed mainly on the identification of genes that are differentially expressed during this developmental transition and/or early in embryo development, and have identified a number of genes whose expression marks or predicts the developmental fate of stressed microspores. More recently, functional genomics approaches have been used to obtain a broad overview of the molecular processes that take place during the establishment of microspore embryogenesis. In this review we summarise accumulated molecular data obtained in rapeseed, tobacco, wheat and barley on embryogenic induction of microspores and define common aspects involved in the androgenic switch.

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Abbreviations

EST:

Expressed Sequence Tag

SSH:

Suppression Subtractive Hybridisation

References

  • Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133(6):1251–1263

    Article  PubMed  CAS  Google Scholar 

  • Bassüner R, Bäumlen H, Hut A, Jung R, Wobus U, Rapoport TA, Saalbach G, Müntz K, (1988) Abundant embryonic mRNA in field bean (Vicia faba L.) codes for a new class of seed proteins: cDNA cloning and characterisation of the primary translation product. Plant Mol Biol 11:321–334

    Article  Google Scholar 

  • Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133(2):713–725

    Article  PubMed  CAS  Google Scholar 

  • Beers EP, Jones AM, Dickerman AW (2004) The S8 serine, C1A cysteine and A1 aspartic protease families in Arabidopsis. Phytochemistry 65:43–58

    Article  PubMed  CAS  Google Scholar 

  • Benito Moreno RM, Macke F, Hauser MT, Alwen A, Heberle-Bors E (1988) Sporophytes and male gametophytes from in vitro-cultured, immature tobacco pollen. In: Cresti M, Jori P, Pacini E (eds), Sexual reproduction in higher plants. Springer, Berlin, pp 137–142

    Google Scholar 

  • Binarova P, Straatman K, Hause B, Hause G, Van Lammeren AAM (1993) Nuclear DNA synthesis during the induction of embryogenesis in cultured microspores and pollen of Brassica napus L. Theor Appl Genet 87:9–16

    Article  CAS  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002). Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  PubMed  CAS  Google Scholar 

  • Boutilier K, Fiers M, Liu C-M, Geest AHM (2004) Biochemical and molecular aspects of haploid embryogenesis. In: Palmer D, Keller W, Kasha K (eds), Haploids in Crop Improvement II. Springer, Heidelberg, pp 73–96

    Google Scholar 

  • Brunel D, Froger N, Pelletier G (1999) Development of amplified consensus genetic markers (ACGM) in Brassica napus from Arabidopsis thaliana sequences of known biological function. Genome 42:387–402

    Article  PubMed  CAS  Google Scholar 

  • Chesnokov YV, Meister A, Manteuffel R (2002) A chimeric green fluorescent protein gene as an embryogenic marker in transgenic cell culture of Nicotiana plumbaginifolia Viv. Plant Sci 162:59–77

    Article  CAS  Google Scholar 

  • Custers JBM, Cordewener JHG, Fiers MA, Maasen BTH, vanLookerenCampagne MM, Liu CM (2001. Androgenesis in Brassica; a model system to study the induction of plant embryogenesis. In: Bhojwani SS, Soh WY (eds) Current trends in the embryology of angiosperms Kluwer Academic Publishers, Dordrecht, pp. 451–470

    Google Scholar 

  • Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    Article  PubMed  CAS  Google Scholar 

  • Fiers M, Hause G, Boutilier K, Casamitjana-Martinez E, Weijers D, Offringa R, van derGeest L, van Lookeren Campagne M, Liu CM (2004) Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene 18:37–49

    Article  CAS  Google Scholar 

  • Garrido D, Vicente O, Heberle-Bors E, Rodriquez-Garcia MI (1995) Cellular changes during the acquisition of embryogenic potential in isolated pollen grains of Nicotiana tabacum. Protoplasma 186:220–230

    Article  Google Scholar 

  • Hattori J, Boutilier K, van Lookeren Campagne MM, Miki BL (1998) A conserved BURP domain defines a novel group of plant proteins with unusual primary structures. Mol Gen Genet 259:424–428

    Article  PubMed  CAS  Google Scholar 

  • Hays DB, Mandel RM, Pharis RP (2001) Hormones in zygotic and microspore embryos of Brassica napus. Plant Growth Regul 35:47–58

    Article  CAS  Google Scholar 

  • Hellmann H, Estelle M (2004) Plant development: regulation by protein degradation. Science 297(5582): 793–797

    Article  Google Scholar 

  • Hobe M, Mülller R, Grünewald M, Brand U, Simon R (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol 213:371–381

    Article  PubMed  CAS  Google Scholar 

  • Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132(2):640–652

    Article  PubMed  CAS  Google Scholar 

  • Ilic-Grubor K, Attree SM, Fowke LC (1998) Comparative morphological study of zygotic and microspore-derived embryos of Brassica napus L. as revealed by scanning electron microscopy Ann Bot 82:157–165

    Article  Google Scholar 

  • Indrianto A, Barinova I, Touraev A, Heberle-Bors E (2001) Tracking individual wheat microspores in vitro: identification of embryogenic microspores and body axis formation in the embryo. Planta 212(2):163–174

    Article  PubMed  CAS  Google Scholar 

  • Jähne A, Becker D, Brettschneider R, Lörz H (1994) Regeneration of transgenic, microspore-derived, fertile barley. Theor Appl Genet 89:525–533

    Article  Google Scholar 

  • Jähne A, Lörz H (1995) Cereal microspore culture. Plant Sci 109:1–12

    Article  Google Scholar 

  • Kyo M, Harada H (1986) Control of the developmental pathway of tobacco pollen in vitro. Planta 168:427–432

    Article  CAS  Google Scholar 

  • Kyo M, Yamaji N, Yuasa Y, Maeda T, Fukui H (2002) Isolation of cDNA coding for NtEPb1-b3, marker proteins for pollen dedifferentiation in a tobacco pollen culture system. Plant Sci 163:1055–1062

    Article  CAS  Google Scholar 

  • Kyo M, Hattori S, Yamaji N, Pechan P, Fukui H (2003) Cloning and characterization of cDNAs associated with the embryogenic dedifferentiation of tobacco immature pollen grains. Plant Sci 164(6):1057–1066

    Article  CAS  Google Scholar 

  • Lee JY, Lee DH (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132(2):517–529

    Article  PubMed  CAS  Google Scholar 

  • Li WZ, Song ZH, Guo BT, Xu LJ (2001) The effects of DNA hypomethylating drugs on androgenesis in barley (Hordeum vulgare l.) in vitro cell. Dev Biol–Plant 37:605–608

    CAS  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257(5072):967–971

    Article  PubMed  CAS  Google Scholar 

  • Maraschin SF, Vennik M, Lamers GEM, Spaink HP, Wang M, (2005a) Time-lapse tracking of barley androgenesis reveals position-determined cell death within pro-embryos. Planta 220(4):531–540

    Article  CAS  Google Scholar 

  • Maraschin SF, Caspers M, Potokina E, Wülfert F, Corredor M, Graner A, Spaink HP, Wang M (2005b) Androgenic switch in barley microspores. II. cDNA array analysis of stress-induced gene expression in barley androgenesis. PhD thesis, Leiden University, The Netherlands

  • Maraschin SF, Priester W de, Spaink HP, Wang M (2005c) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56:1711–1726

    Google Scholar 

  • Maraschin SF, Gaussand G, Olmedilla A, Pulido A, Lamers GEM, Korthout H, Spaink HP, Wang M (2005d) Programmed cell death during the transition from multicellular structures into globular embryos in barley androgenesis. Planta 221:459–470

    Google Scholar 

  • Rays DB, Reid DM, Yeung EC, Pharis RP (2000) Role of ethylene in cotyledon development of microspore-derived embryos of Brassica napus. J Exp Bot 51:1851–1859

    Article  Google Scholar 

  • Reynolds TL, Kitto S (1992) Identification of embryoid-abundant genes that are temporally expressed during pollen embryogenesis in wheat anther cultures. Plant Physiol 100:1744–1750

    Article  PubMed  CAS  Google Scholar 

  • ReynoldsTL, Crawford RL (1996) Changes in abundance of an abscisic acid-responsive, early cysteine- labeled metallothionein transcript during pollen embryogenesis in bread wheat (Triticum aestivum L.). Plant Mol Biol 32:823–829

    Article  Google Scholar 

  • Reynolds TL (2000) Effects of calcium on embryogenic induction and the accumulation of abscisic acid, and an early cysteine-labeled metallothionein gene in androgenic microspores of Triticum aestivum. Plant Science 150:201–207

    Article  CAS  Google Scholar 

  • Sagerström CG, Sun BI, Sive HL (1997) Subtractive cloning: past, present and future. Annu Rev Biochem 6:751–783

    Article  Google Scholar 

  • Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F, Grignon C (1992) Cloning and expression of a plant potassium ion transport system. Science 256:663–665

    Article  PubMed  CAS  Google Scholar 

  • Touraev A, Ilham A, Vicente O, Heberle-Bors E (1996a) Stress induced microspore embryogenesis from tobacco microspores: an optimized system for molecular studies. Plant Cell Rep 15:561–565

    Article  CAS  Google Scholar 

  • Touraev A, Indrianto A, Wratschko I, Vicente O, Heberle-Bors E (1996b) Efficient microspore embryogenesis in wheat (Triticum aestivum.L) induced by starvation at high temperatures. Sex Plant Reprod 9:209–215

    Article  Google Scholar 

  • Touraev A., Vicente O, Heberle-Bors E 1997. Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:285–303

    Article  Google Scholar 

  • Touraev A, Heberle-Bors E (1999) Microspore embryogenesis and in vitro pollen maturation in tobacco. In: Hall RD (eds), Methods in molecular biology, vol. III, plant cell culture protocols, Humana Press, Totowa, New Jersey, pp 281–291

    Chapter  Google Scholar 

  • Touraev A, Pfosser M, Heberle-Bors E (2001) The microspore: a haploid multipurpose cell. In: Adv Bot Res 35:53–109

    Google Scholar 

  • Theocharis SE, Margeli AP, Koutselinis A (2003) Metallothionein: a multifunctional protein from toxicity to cancer. Int J Biol Markers 18 (3):162–169

    PubMed  CAS  Google Scholar 

  • Vrinten PL, Nakamura T, Kasha KJ (1999) Characterization of cDNAs expressed in the early stages of microspore embryogenesis in barley (Hordeum vulgare L.) L. Plant Mol Biol 41(4):455–463

    Article  PubMed  CAS  Google Scholar 

  • Weselake RJ (2000) Lipid biosynthesis in cultures of oilseed rape. In Vitro Cell Dev Biol –Plant 36:338–348

    Article  CAS  Google Scholar 

  • Wysocki R, Kron SJ (2004) Yeast cell death during DNA damage arrest is independent of caspase or reactive oxygen species. J Cell Biol 166(3):311–316

    Article  PubMed  CAS  Google Scholar 

  • Yeung EC, Rahman MH, Thorpe TA (1996) Comparative development of zygotic and microspore-derived embryos in Brassica napus L. cv Topas. I. Histodifferentiation. Int J Plant Sci 157:27–39

    Article  Google Scholar 

  • Zarsky V, Garrido D, Rihova L, Tupy J, Vicente O, Heberle-Bors E (1992) Derepression of the cell cycle by starvation is involved in the induction of tobacco pollen embryogenesis. Sex Plant Reprod 5:189–194

    Article  Google Scholar 

  • Zoriniants S, Tashpulatov AS, Heberle-Bors E, Touraev A (2005) The role of stress in the induction of haploid microspore embryogenesis. In: Palmer D Keller W Kasha K (eds), Haploids in crop improvement II, Springer, Heidelberg. pp 35–52

    Chapter  Google Scholar 

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Correspondence to Alisher Touraev.

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Hosp, J., de Maraschin, S.F., Touraev, A. et al. Functional genomics of microspore embryogenesis. Euphytica 158, 275–285 (2007). https://doi.org/10.1007/s10681-006-9238-9

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