The Library

Regulation of seed germination in the close Arabidopsis relative Lepidium sativum : a global tissue-specific transcript analysis

Tools

Morris, Karl, Dr., Linkies, Ada, Müller, Kerstin, Oracz, Krystyn, Wang, Xiaofen, Lynn, James R. , Leubner-Metzger, Gerhard and Finch-Savage, William E.. (2011) Regulation of seed germination in the close Arabidopsis relative Lepidium sativum : a global tissue-specific transcript analysis. Plant physiology, Vol.155 (No.4). pp. 1851-1870. ISSN 1532-2548

Preview

PDF
WRAP_Morris_1851.full.pdf - Published Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (2114Kb)

Official URL: http://dx.doi.org/10.1104/pp.110.169706

Abstract

The completion of germination in Lepidium sativum and other endospermic seeds (e.g. Arabidopsis [Arabidopsis thaliana]) is regulated by two opposing forces, the growth potential of the radicle (RAD) and the resistance to this growth from the micropylar endosperm cap (CAP) surrounding it. We show by puncture force measurement that the CAP progressively weakens during germination, and we have conducted a time-course transcript analysis of RAD and CAP tissues throughout this process. We have also used specific inhibitors to investigate the importance of transcription, translation, and posttranslation levels of regulation of endosperm weakening in isolated CAPs. Although the impact of inhibiting translation is greater, both transcription and translation are required for the completion of endosperm weakening in the whole seed population. The majority of genes expressed during this process occur in both tissues, but where they are uniquely expressed, or significantly differentially expressed between tissues, this relates to the functions of the RAD as growing tissue and the CAP as a regulator of germination through weakening. More detailed analysis showed that putative orthologs of cell wall-remodeling genes are expressed in a complex manner during CAP weakening, suggesting distinct roles in the RAD and CAP. Expression patterns are also consistent with the CAP being a receptor for environmental signals influencing germination. Inhibitors of the aspartic, serine, and cysteine proteases reduced the number of isolated CAPs in which weakening developed, and inhibition of the 26S proteasome resulted in its complete cessation. This indicates that targeted protein degradation is a major control point for endosperm weakening.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Germination, Lepidium -- Genetics, Endosperm
Journal or Publication Title:	Plant physiology
Publisher:	American Society of Plant Biologists
ISSN:	1532-2548
Date:	April 2011
Volume:	Vol.155
Number:	No.4
Page Range:	pp. 1851-1870
Identification Number:	10.1104/pp.110.169706
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Deutsche Forschungsgemeinschaft (DFG), Deutscher Akademischer Austauschdienst (DAAD), Wissenschaftliche Gesellschaft in Freiburg i.B., Natural Science Foundation of Guangdong Province (NSFGP), Alexander von Humboldt-Stiftung (AvHS)
Grant number:	BB/E006418/1 (BBSRC), LE720/6 (DFG), D/0628197 (DAAD), 07006658 (NSFGP), MU3114/ 1–1 (DFG)
References:	Allemeersch J, Durinck S, Vanderhaeghen R, Alard P, Maes R, Seeuws K, Bogaert T, Coddens K, Deschouwer K, Van Hummelen P, et al (2005) Benchmarking the CATMA microarray: a novel tool for Arabidopsis transcriptome analysis. Plant Physiol 137: 588–601 Arana MV, de Miguel LC, Sa´nchez RA (2006) A phytochrome-dependent embryonic factor modulates gibberellin responses in the embryo and micropylar endosperm of Datura ferox seeds. Planta 223: 847–857 Arcila J, Mohapatra SC (1992) Effect of protein-synthesis inhibitors on tobacco seed-germination and seedling emergence. J Plant Physiol 139: 460–466 Bar-Or C, Czosnek H, Koltai H (2007) Cross-species microarray hybridizations: a developing tool for studying species diversity. Trends Genet 23: 200–207 Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150: 1006–1021 Becnel J, Natarajan M, Kipp A, Braam J (2006) Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol Biol 61: 451–467 Beers EP, Jones AM, Dickerman AW (2004) The S8 serine, C1A cysteine and Al aspartic protease families in Arabidopsis. Phytochemistry 65: 43–58 Belotserkovsky H, Berger Y, Shahar R, Wolf S (2007) Specific role of LeMAN2 in the control of seed germination exposed by overexpression of the LeMAN3 gene in tomato plants. Planta 227: 199–209 Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289–300 Berger D, Altmann T (2000) A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev 14: 1119–1131 Bethke PC, Libourel IGL, Aoyama N, Chung YY, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143: 1173–1188 Bewley JD (1997) Breaking down the walls: a role for endo-b-mannanase in release from seed dormancy? Trends Plant Sci 2: 464–469 Bourgault R, Bewley JD (2002) Gel diffusion assays for endo-b-mannanase and pectin methylesterase can underestimate enzyme activity due to proteolytic degradation: a remedy. Anal Biochem 300: 87–93 Broadley MR, White PJ, Hammond JP, Graham NS, Bowen HC, Emmerson ZF, Fray RG, Iannetta PPM, McNicol JW, May ST (2008) Evidence of neutral transcriptome evolution in plants. New Phytol 180: 587–593 Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J 53: 214–224 Carrera E, Holman T, Medhurst A, Peer W, Schmuths H, Footitt S, Theodoulou FL, Holdsworth MJ (2007) Gene expression profiling reveals defined functions of the ATP-binding cassette transporter COMATOSE late in phase II of germination. Plant Physiol 143: 1669–1679 Cervantes E, Rodrı´guez A, Nicola´s G (1994) Ethylene regulates the expression of a cysteine proteinase gene during germination of chickpea (Cicer arietinum L.). Plant Mol Biol 25: 207–215 Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 113–116 Chen F, Bradford KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiol 124: 1265–1274 Chen F, Nonogaki H, Bradford KJ (2002) A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination. J Exp Bot 53: 215–223 Choi D, Cho HT, Lee Y (2006) Expansins: expanding importance in plant growth and development. Physiol Plant 126: 511–518 Comai L, Dietrich RA, Maslyar DJ, Baden CS, Harada JJ (1989) Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L. Plant Cell 1: 293–300 Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850–861 Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651–679 da Silva EAA, Toorop PE, Nijsse J, Bewley JD, Hilhorst HWM (2005) Exogenous gibberellins inhibit coffee (Coffea arabica cv. Rubi) seed germination and cause cell death in the embryo. J Exp Bot 56: 1029–1038 da Silva EAA, Toorop PE, van Aelst AC, Hilhorst HWM (2004) Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Coffea arabica cv. Rubi) seed germination. Planta 220: 251–261 Debeaujon I, KoornneefM(2000) Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiol 122: 415–424 Debeaujon I, Le´on-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122: 403–414 de Miguel L, Burgin MJ, Casal JJ, Sa´nchez RA (2000) Antagonistic action of low-fluence and high-irradiance modes of response of phytochrome on germination and beta-mannanase activity in Datura ferox seeds. J Exp Bot 51: 1127–1133 Dhugga KS, Barreiro R,Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, et al (2004) Guar seed betamannan synthase is a member of the cellulose synthase super gene family. Science 303: 363–366 Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin- induced degradation of RGA. Proc Natl Acad Sci USA 98: 14162– 14167 Edwards ME, Choo TS, Dickson CA, Scott C, Gidley MJ, Reid JSG (2004) The seeds of Lotus japonicus lines transformed with sense, antisense, and sense/antisense galactomannan galactosyltransferase constructs have structurally altered galactomannans in their endosperm cell walls. Plant Physiol 134: 1153–1162 Feurtado JA, Banik M, Bewley JD (2001) The cloning and characterization of alpha-galactosidase present during and following germination of tomato (Lycopersicon esculentum Mill.) seed. J Exp Bot 52: 1239–1249 Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171: 501–523 Finkelstein R, ReevesW, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59: 387–415 Franzke A, German D, Al-Shehbaz IA, Mummenhoff K (2009) Arabidopsis family ties: molecular phylogeny and age estimates in Brassicaceae. Taxon 58: 425–437 Frugis G, Chua NH (2002) Ubiquitin-mediated proteolysis in plant hormone signal transduction. Trends Cell Biol 12: 308–311 Fry SC (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytol 161: 641–675 Fry SC, Dumville JC, Miller JG (2001) Fingerprinting of polysaccharides attacked by hydroxyl radicals in vitro and in the cell walls of ripening pear fruit. Biochem J 357: 729–737 Fujikura Y, Karssen CM (1995) Molecular studies on osmoprimed seeds of cauliflower: a partial amino-acid-sequence of a vigor-related protein and osmopriming-enhanced expression of putative aspartic protease. Seed Sci Res 5: 177–181 Gaete-Eastman C, Figueroa CR, Balbontin C, Moya M, Atkinson RG, Herrera R, Moya-Leon MA (2009) Expression of an ethylene-related expansin gene during softening of mountain papaya fruit (Vasconcellea pubescens). Postharvest Biol Technol 53: 58–65 Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA 99: 11519–11524 Gong XM, Bewley JD (2007) Sorting out the LeMANs: endo-beta-mannanase genes and their encoded proteins in tomato. Seed Sci Res 17: 143–154 Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399–3414 Hartweck LM (2008) Gibberellin signaling. Planta 229: 1–13 Helm M, Schmid M, Hierl G, Terneus K, Tan L, Lottspeich F, Kieliszewski MJ, Gietl C (2008) KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds. Am J Bot 95: 1049–1062 Hilson P, Allemeersch J, Altmann T, Aubourg S, Avon A, Beynon J, Bhalerao RP, Bitton F, Caboche M, Cannoot B, et al (2004) Versatile gene-specific sequence tags for Arabidopsis functional genomics: transcript profiling and reverse genetics applications. Genome Res 14: 2176–2189 Holdsworth MJ, Bentsink L, Soppe WJJ (2008a) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179: 33–54 Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008b) Postgenomics dissection of seed dormancy and germination. Trends Plant Sci 13: 7–13 Hughes DW, Galau GA (1989) Temporally modular gene expression during cotyledon development. Genes Dev 3: 358–369 Hughes DW, Galau GA (1991) Developmental and environmental induction of Lea and LeaA mRNAs and the postabscission program during embryo culture. Plant Cell 3: 605–618 Iglesias-Ferna´ndez R, Matilla A (2009) After-ripening alters the gene expression pattern of oxidases involved in the ethylene and gibberellin pathways during early imbibition of Sisymbrium officinale L. seeds. J Exp Bot 60: 1645–1661 Iglesias-Ferna´ndez R, Rodrı´guez-GacioMC, Barrero-Sicilia C, Carbonero P, Matilla A (2011) Three endo-b-mannanase genes expressed in the micropylar endosperm and in the radicle influence germination of Arabidopsis thaliana seeds. Planta 233: 25–36 Ikuma H, Thimann KV (1963) The role of the seed-coats in germination of photosensitive lettuce seeds. Plant Cell Physiol 4: 169–185 Itai A, Ishihara K, Bewley JD (2003) Characterization of expression, and cloning, of beta-D-xylosidase and alpha-L-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit. J Exp Bot 54: 2615–2622 Jendrisak J (1980) The use of alpha-amanitin to inhibit in vivo RNA synthesis and germination in wheat embryos. J Biol Chem 255: 8529–8533 Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20: 1260–1277 Kimura M, Nambara E (2010) Stored and neosynthesized mRNA in Arabidopsis seeds: effects of cycloheximide and controlled deterioration treatment on the resumption of transcription during imbibition. Plant Mol Biol 73: 119–129 Knox JP (2008) Mapping the walls of the kingdom: the view from the horsetails. New Phytol 179: 1–3 Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15: 281–307 Leubner-Metzger G (2002) Seed after-ripening and over-expression of class I beta-1,3-glucanase confer maternal effects on tobacco testa rupture and dormancy release. Planta 215: 959–968 Leubner-Metzger G (2003) Functions and regulation of beta-1,3-glucanases during seed germination, dormancy release and after-ripening. Seed Sci Res 13: 17–34 Liepman AH, Wilkerson CG, Keegstra K (2005) Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases. Proc Natl Acad Sci USA 102: 2221–2226 Lim PO, Kim Y, Breeze E, Koo JC, Woo HR, Ryu JS, Park DH, Beynon J, Tabrett A, Buchanan-Wollaston V, et al (2007) Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J 52: 1140–1153 Linkies A, Mu¨ ller K, Morris K, Tureckova´ V, Wenk M, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, et al (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21: 3803–3822 Liu Z, Karmarkar V (2008) Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci 13: 137–144 Lizana XC, Riegel R, Gomez LD, Herrera J, Isla A, McQueen-Mason SJ, Calderini DF (2010) Expansins expression is associated with grain size dynamics in wheat (Triticum aestivum L.). J Exp Bot 61: 1147–1157 Lopez-Molina L, Mongrand S, Kinoshita N, Chua N-H (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17: 410–418 Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, et al (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64: 191–203 Maris A, Suslov D, Fry SC, Verbelen JP, Vissenberg K (2009) Enzymic characterization of two recombinant xyloglucan endotransglucosylase/ hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension. J Exp Bot 60: 3959–3972 Mella RA, Burgin MJ, Sanchez RA (2004) Expansin gene expression in Datura ferox L. seeds is regulated by the low-fluence response, but not by the high-irradiance response, of phytochromes. Seed Sci Res 14: 61–71 Mo BX, Bewley JD (2002) Beta-mannosidase (EC 3.2.1.25) activity during and following germination of tomato (Lycopersicon esculentum Mill.) seeds: purification, cloning and characterization. Planta 215: 141–152 Mu¨ ller K, Job C, Belghazi M, Job D, Leubner-Metzger G (2010) Proteomics reveal tissue-specific features of the cress (Lepidium sativum L.) endosperm cap proteome and its hormone-induced changes during seed germination. Proteomics 10: 406–416 Mu¨ ller K, Linkies A, Vreeburg RAM, Fry SC, Krieger-Liszkay A, Leubner-Metzger G (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150: 1855–1865 Mu¨ ller K, Tintelnot S, Leubner-Metzger G (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 47: 864–877 Mutlu A, Chen X, Reddy SM, Gal S (1999) The aspartic proteinase is expressed in Arabidopsis thaliana seeds and localized in the protein bodies. Seed Sci Res 9: 75–84 Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41: 697–709 Neuteboom LW, Veth-Tello LM, Clijdesdale OR, Hooykaas PJ, van der Zaal BJ (1999) A novel subtilisin-like protease gene from Arabidopsis thaliana is expressed at sites of lateral root emergence. DNA Res 6: 13–19 Nonogaki H, Chen F, Bradford K (2007) Mechanisms and genes involved in germination sensu stricto. In K Bradford, H Nonogaki, eds, Seed Development, Dormancy and Germination. Blackwell, Oxford, pp 264–304 Nonogaki H, Gee OH, Bradford KJ (2000) A germination-specific endo-bmannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiol 123: 1235–1246 Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15: 1591–1604 Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka M, Endo TA, Mochizuki Y, Toyoda T, Kamiya Y, et al (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62: 39–51 Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pe´rez AC, Chico JM, Bossche RV, Sewell J, Gil E, et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464: 788–791 Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol 15: 1998–2006 Penfield S, King J (2009) Towards a systems biology approach to understanding seed dormancy and germination. Proc Biol
URI:	http://wrap.warwick.ac.uk/id/eprint/34857