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Molecular & Cytological Aspects of Seed Development in Sexual k"8. Molecular & cytological aspects of seed development in sexual & apomictic Hierqcium by Matthew Robert Tucker B. Biotech (Hons) A thesis submitted for the degree of Doctor of Philosophy af The University of Adelaide, Department of Agricultural Science in collaboration with CSIRO Plant Industry, Horticulture lJnit LJrrbrae, Adelaide April zo'n 2003 II CONTENTS Molecular & cytological aspects of seed development in sexual & apomictic Hierqcium,............ I Abstract.. VI Declaration VIII Acknowledgements """"""""' IX Publications 1 Chapter 1: Molecular and cytological aspects of early seed development........'......'.'........'..........2 A. Preliminary Comments.., """"""""""'2 1.1 Introduction """""""""""f 1.2 Ontogeny ofseed development in sexualþ teproducing plants""""" 5 1.2.1 Early ovule development 6 1.2.2 Embryo sac development - megaspologenesrs.'.. 1 1.2.3 Embryo sac development - megagametogenesis and matulity. 8 r.2.4 Post-fertilisation seed development 9 1.2.5 Embryo development t.2.6 Endosperm development 1.2.7 The role of the endospetm in seed development..'......'.' t.2.8 Molecular controls of endosperm formation - the Arabidopsls FIS genes . ... 1.3 Apomixis: asexual reprodttction through seed. 22 l.3.1 Types of apomixis....'. 23 1.4 Hierøcium is ø model apomictic plant...'..'..-....... """"""""""""26 1.4.1 Initiation of apospoly in Hieracium 1.4.2 Aposporous embryo sac developmentin Hieraciunt 1.5 Endosperm formution in facultative øpomicts ....'. 1.5.1 Formation of pseudogamous endosperm.....'......'..... I.5.2 Formation of fertilisation-independent (autonomous) endosperm 1.6 Genetic control of apomixis. """""""32 1.7 Models for the control of apomixis.. 33 34 1.7 .I Hybridisation of related species 35 1.7 .2 Mutation of a key regulatory gene(s) ir't .3 Epigenetic regulation of gene expression,...... 35 36 1.1 .4 Apomixis-specific factors - "alien" DNA ..'..' 1.8 Addressing questions of tpomkis in Hierøcium """"""""""""'37 1.9 Specific thesis aims """"18 il Chapter 2: Cytological characterisation of early seed development in sexual and apomictic 2.1 Introduction...,'..'..','. """""'40 2,2 Materitls and Methods """'42 2.3 Results 44 2.3.1 Early seed development in sexual P4 Hieracium 44 2.3.2 Early seed development in apomictic D3 Hieracium 41 5r 2.3.3 Abnormalities during seed development in apomictic D3 ........" """ ' 2.3.4 Tracking seed vatiability during development in apomictic D3 """"' 52 2.3.s Ploidy analysis of mature Hieracium seeds ........... .54 2.3.6 variable ploicly levels in mature seeds ffom apomictic D3 Hieraciunt .56 2.4 Discussion. 58 2.4.r Early divisions of the embryo sac and endosperm are alteled in apomictic D3 Hieracium5S 2.4.3 Cellular endosperm is required for embryo growth to rnaturity in apomictic D3 Hieracium 2.4.4 Multiple origins of the endosperm and embryo in apomictic D3 Hieracium. 2.4.5 Moleôular identity of endosperm cells in apomictic and sexual Hieracium... Chapter 3: ATMEA:GUS,AIFIS2:GUS andAtFIE GUS expression during seed development in ."*oil and apomictic Hieracium """""""""68 3.1 Introduction """""""""'ó8 3.2 Materials ønd Methods """""""""""70 3,3 Results """ 73 3.3.1 ATFIS:GUS gene expression marks mature embryo sacs and initiating seed structures in sexual H ieracium ............ 14 3.3.2 Conservation of ATFIS;GUS expression in sexual and apomictic Hieracium 16 3.3.3 A\FIS2:GUS marks megaspores and is down-regulated in the selected megaspore... 78 3.3.4 AIFIS2;GUS is differentially expressed at meiosis in apomictic Hieracium.........""' 80 3.4 Discussion... 3.4.1 Apomixis reflects a deregulated sexual program ...'......."'... 3.4.2 A simple model for the regulation of apomixis in Hieracium 3.4.3 Interaõüons between spofophytic tissues, sexual and apomictic pathways. 3.4.4 Roles ol F/S-class genes in apomictic reproduction Chapter 4: Isolation of Arabidopsis enhancer trap tagged promoters and characterisation of their expression during megagametogenesis and seed development """""""""' 87 4.1 Introduction """""""""'87 4.2 Møterittls und Methods """"""""""" 88 4.3 Results """""""""""""'91 4.3.1 Insertion sites of five ETs in the Afabidopsis genon're and their expression characteristics9l .............95 4.3 .2 Four of the six tested chimeric marker genes were not expressed in floral tissues 4.3.3 Expression of Atl8l l:GUS was detected in vascular tissues.......... ...............95 4.3.4 Expression of At2209-l:GUS was detected in synelgids and antipodal cells in Arabidopsis ovules. 96 4.3,5 Expression of At2209-1:GUS was not detected in apomictic D3 Hieracium'. ..."'...,. ..91 4.4 Discttssion... 99 IV 4.4.1 Proximal promoter sequences do not regulate the ovule exptessiou ol five Arrtbidopsis enhancer tlap lines 4.4.2 The AtL04L'GUS gene lacks ovule regulatory sequences.'., 4.4.3 Atl811:GUS is a vascular tissue marker gene'...... 4.4.4 At2209-1:GUS is a synergid and antipodal cell marker gene 4.4.5 Enhancer traps and cell identity in apomictic Hieraciuru ..... Chapter 5: Identification of cDNAs from Hierøcium encoding putative regulators of gamãtophyte and seed development..'................ """"""106 5.1 Introduction ,""""""""106 5.2 Mflteriols and Methods ...-,.....'.'.'.'."108 5.3 Results 114 5.3.I Low abundance clones from an early Hieracium ovule cDNA library tt4 115 5 .3 .2 Putative identity of HOS clones .... ...... 5.3.3 Candidate genes regulating cell-specification and developmental processes in early Hieracium ovules ..118 5.3.4 Isolation of early seed regulators from Hieracium.... ..118 5.4 Discussion... ................. 127 5.4.1 Identification ol Hieracium Ovule Sequence (HOS) genes.... .... ..,""""121 5.4.2 Identification of CLAVATA| (CLVl)-like genes from eally Hieracium ovaries...........,...129 5.4.3 The HMET and HHDAC clones are tools fol the investigation of epigenetic gene legulation in Hieracium ........................130 5.4.4 FIS2-llke genes in Hierqcium """'132 5.4.5 Conserved FIE-llke genes exist in sexual and apomictic Hieracium. """....134 Chapter 6: Characterisation of Hierucium F1E genes .................'.""136 6.1 Introduction .................136 6.2 Materiøls and Methods '-'..-'.'...".'."'137 6.3 Results ..-',.'-.,..."."'.'.'.'141 6.3.1 Design of acomplementation strategy for the Arabidopsisfie-2 mutant..........................141 6.3.2 Complementation of Arabidopsis fie-2 with the D3 HFIE cDNA .'.,",. """143 6.3.3 Isolaiion of HFIE promoter sequences from Hieraciwnby ptomoter walking... ..............146 6.3.4 Comparison of genomic regions ín the HFIE promoters . ". " ' 148 6.3.5 Identification of HFIE promoter sequences by spanning PCR .........'.' "'.""149 6.3.6 Phylogenetic comparison of the D3 and P4 HFIE sequences.........'.. .' ." " 151 6.3.1 Preliminary analysis of HFIE:GUS expression patterns . "'152 6.3.8 Further characterisation of the D3 HFIES retroelement. ..,. "154 6.4. t D3-cHFIE encodes a functional V/D-40 Polycomb group (PcC) protein ..155 6.4.4 Retroelements and increased chromosomal DNA levels in apomictic Hieracium.. 161 6.4.5 Elucidation of endogenous HFIE function in sexual and apomictic plants r64 Chapter 7: Silencing of FIE genes in sexual and apomictic Ilierøcium 166 7.1 Introduction """"""""'166 7.2 Materiols ønd Methods ."',"""""""'167 7.3 Results 170 '7 .3.r Generation of 355:HFIE'RNAi and MEA:HFIE:RNAI transgenic lines 170 7.3.2 plants........ 7.3.3 i lines.......' 7 .3.4 line #7 ...... 1.3.5 Embryo sacs and embryos abort in 355:HFIE:RNAI lines #5 and#l 7.3.6 P4 3iS:HFIE;RNAI line #4 does not develop endosperm without f'ertilisation ....,.. 7.4 Discussion... 180 180 1 .4.1 RNAi constructs silence gene expression tn Hieracium .'....'....". \82 1 .4.2 Down-regulation of HFIE in apomictic Hieracium alters plant development '7 .4.3 Promoter limitations may effect the penetrance of phenotypes in Hieracium 183 3 5 S : HFIE: RNAI lines........... 1 .4.4 Down-regulation of HFIE in vegetative tissues alters Hieracium ::111 :::: Ït:::-::i ï i::-l:i;. j .4.5 Down-regulation of HFIE in developing seeds alters late seed development in apomictic Hieracium .......194 j .4.6 MES-6,The C. elegans homolog of EXTRA SEX COMBS (Esc) and FIE, is required for RNAi silencing.. 185 7.4.1 Functional models for the HFIS PcG complex ... 187 Chapter 8: Summary and Concluding Discussion.'.....'.......'.. """""'189 Appendix 1: Stages offlorat development in Hierucium """""""""""195 Appendix 2: Contents of høematoxylin stained seeds.......,-,., """""""' 196 Appendk 3: Primers and PCR Conditions... """"""""""198 Bibliography 202 VI Abstract Sexual reproduction in angiosperms is a highly regulated process that begins with the formation of a flower and ends with the formation of seeds. The ovule is the progenitor of the seed and during the course of reproduction it is the site of embryo sac formation, double fertilisation and embryo and endosperm development. Asexual seed reproduction in Hieracium, referred to as apomixis, is characterised by the formation of an embryo sac(s) without meiosis, and an embryo and endosperm without fertilisation. The molecular processes controlling apomixis are unknown. In this study, molecular and cytological aspects of fertilisation-independent (autonomous) endosperm development were investigated tn Hieracium. Early autonomous endosperm divisions were irregular in the apomict when compared to fertilisation-dependent endosperm divisions in the sexual plant. However, the general morphology of dividing syncytial nuclei and endosperm cells, and the expression patterns of the ATMEA:GUS, AIFIS2;GUS and
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