maternal control of seed development -...

doi:10.1006/scdb.2001.0267, available online at http://www.idealibrary.com onseminars in CELL & DEVELOPMENTAL BIOLOGY , Vol. 12, 2001: pp. 381–386

Maternal control of seed development

Abdul M. Chaudhury a,∗ and Frederic Berger b

Maternal control of higher plant seed development islikely to involve female sporophytic as well as femalegametophytic genes. While numerous female sporophyticmutants control the production of the ovule and the embryosac true maternal effect mutations affecting embryo andendosperm development are rare in plants. A new class offemale gametophytic mutants has been isolated that controlsautonomous development of endosperm. Molecular analysesof these genes, known as FIS class genes, suggest that theyrepress downstream seed development genes by chromatinremodelling. Expression of the FIS genes in turn is modulatedby parent specific expression or genomic imprinting whichin turn is controlled by DNA methylation. Thus maternalcontrol of seed development is a complex developmental eventinfluenced by both genetic and epigenetic processes.

Key words: FIS genes / endosperm / embryo / imprinting/ epigenetic / methylation

c© 2001 Academic Press

Introduction

Higher plants are characterized by a complexlife cycle that consists of alternating haploid anddiploid generations. The diploid life form, termedsporophytic, supports meiosis that produces thehaploid male and female spores and initiates thegametophytic generation. The female sporophytealso supplies the maternal structures such as theinteguments within which the seed is nurtured(reviewed in Reference 1). Gametogenesis andfertilization take place in an environment where

From the aCSIRO Plant Industry, GPO BOX 1600 ACT 2601, Aus-tralia and bRDP, UMR 9938, 46 allee d’Italie, 69364 Lyon cedex 07,France. *Corresponding author. E-mail: [email protected]

c©2001 Academic Press1084–9521/01/050381+ 06/$35.00/0

gametophytic and sporophytic structures interactand are placed under several layers of haploid anddiploid genetic controls.1

This interaction culminates in the formation of anew diploid generation during a complex processcalled double fertilization.2 Following female meiosisthree out of the four spores degenerate and thesurviving spore produces a female gametophyte(embryo sac), which contains eight nuclei and sevencells. Two cells are female gametes, the haploidegg cell and the homodiploid central cell. Thehaploid product of male meiosis (pollen) produces atip-growing pollen tube on the sporophytic receptivestigma and eventually enters the ovule through themicropyle (sporophytic) and delivers two sperms intothe embryo sac. Following fusion of these two spermcells two zygotic products are produced, the diploidembryo zygote that develops as the daughter plantand a triploid cell that develops as endosperm.3,4

Higher plant reproduction is thus characterizedby the involvement of five developmental phases,the diploid sporophytic mother, the haploid femalegametophyte, the haploid male gametophyte, thedeveloping diploid embryo and the developingtriploid endosperm. The development of the embryosac and the seed are under the direct maternalcontrols of both the sporophytic and the femalegametophytic origin. The paternal gametophytic andpost-fertilization sporophytic controls are other levelsin the complex genetic interactions that govern seeddevelopment.

Female sporophytic control of embryo sacdevelopment

There are two ways whereby the embryo sac develop-ment can be maternally controlled. First, the develop-ment of the megaspore mother cell and meiosis areunder direct sporophytic control of female specificgenes. Defects caused by these mutations cannot berescued by pollination and thus the lesions are by def-

381

A. M. Chaudhury and F. Berger

inition maternal, although they may not be formallymaternal-effect genes.5,6 A number of mutants haverecently been isolated, including ones that affect fe-male meiosis and the corresponding genes have beencloned.7,8 The mutants belonging to this class showthat female gametophytic development is under thegenetic control of the mother sporophyte.

Maternal effect genes in seed development

Egg cells from flowering plants contain a relativelysmall amount of cytoplasm compared with animalegg cells. Thus asymmetrically distributed maternallyderived gene products may not be as importantin setting up polarized information in the plantembryo. Indeed embryogenesis in plants can occursomatically; thus there may not be a very elaboratematernal program to control the zygotic componentof seed development. Some key genes in maternalcontrol are being discovered using mutational studiesas well as through transgenic studies involving specificregulatory genes.

A true maternal effect embryo lethal mutationwould show an impaired phenotype irrespectiveof the genotype of the zygotic embryo. In sucha recessive mutant even a homozygous mutantembryo would be able to grow if the sporophyteis heterozygous. In contrast, even a heterozygousembryo would be defective if the seed-carryingmother is homozygous for the mutation. A maternaleffect embryo lethal mutation can be identified as afemale sterile plant in which embryo developmentis arrested even if the egg is fertilized with pollencarrying a normal allele. However as shown latergenomic imprinting makes the genetic identificationof true maternal mutation problematic.

Maternal effect is often shown by an impairedfunction of the maternal structures that nourishthe seed. The outermost cell layers of the plantseed are the seed coats that are derived from theovule integument and are of sporophytic maternalorigin. A number of mutants altering differentfeatures of the seed coat have been described. Someof these mutations that affect the development ofthe integument also affect embryo and endospermdevelopment. These include mutants that affectthe function of the maternal tissues involved inthe control of nutrient flow into the endosperm.Such mutants were initially described in Barley.9

In mutants seg1, seg3, seg6 and seg7, the chalazalmaternal transmitting tissue becomes necrotic

and as a consequence, the supply of nutrient ispresumably cut off and reserve storage in theendosperm is prevented, ultimately causing seedlethality. More recently, two mutants belonging to asimilar phenotypic class have been analysed at themolecular level in maize. In this species, a specializedtype of cell, transfer cell has been described in theendosperm.10 These cells form the transfer layerthat overlays the chalaza where vascular tissuesdeliver nutrients. Endosperm transfer cells expressa specific invertase INCW211 and small peptidesBETL1-4.12 The mutants reduced grain-filling-113 andminiature114 show degeneration of the maternalchalaza. Miniature1 encodes an invertase and itsmutation probably causes an imbalance in source–sink relationships in the seed. Interestingly, thedegeneration of the maternal tissue is paralleledwith a decreased expression of BETL genes inthe endosperm, thus showing a direct maternalsporophytic control of endosperm development.

The phenotypes of the sin1 mutants in Arabidopsis 15

and down-regulation of the expression of the genesFBP7 and FBP1116 in Petunia have shown evidenceof maternal sporophytic controls that are probablynot related to seed nutrition. The mutant sin1 showspleiotropic defects in plant development, includingabnormal integuments, delayed flowering time andembryo formation.15,17 Homozygous sin1 motherplants produce seeds that show various embryodefects that include abnormal development of themeristems and the development of single or fusedcotyledons instead of two. The maternal expressionof wild-type SIN1 function seems to be crucial fornormal embryo development establishing SIN1 asa bona fide maternal effect gene. SIN1 encodes amultidomain protein with a DEAH box RNA helicaseC motif, a STAUFEN-like double stranded RNAbinding motif, and a novel conserved motif alsofound in ZWILLE/ARGONAUT and the silencingfactor RDE1. It is thus probable that SIN1 is involvedin post-transcriptional regulation, which could berelated to the pleiotropic phenotype associatedwith sin1 mutants (A. Ray, unpublished, pers com).Interestingly SIN1 is the same as the Carpel Factory(CAF ) gene, required for normal cell division in thefloral meristem.18

Maternal effect has also been identified by acandidate gene strategy in transgenic plants. FLORALBINDING PROTEIN 7 (FBP7) and FBP11 genesencode MADS box protein, a family of transcriptionfactors and are expressed in the ovule integuments.Ectopic expression of FBP7 caused co-supression

382


of both FBP7 and FBP11 and caused abnormalendosperm development. This is likely due to acell non-autonomous effect since pollination ofplants that exhibit co-suppression of FBP7/11 withwild-type pollen does not rescue the abnormalendosperm development.16 In seeds developingfrom the reciprocal cross, in which the co-suppressedgenome is derived paternally and the female parentcontains normal FBP7 and FBP11 loci, endospermdevelopment was normal. Thus normal maternalexpression of FBP7 and FBP11 seems to be requiredfor normal endosperm development. Togetherwith sin1, these reports represent some of the fewexamples published to date of maternal sporophyticeffects on endosperm or embryo development.

Paternal silencing during early embryodevelopment; a genome-wide maternal effect?

Conventional Mendelian genetics assumes that bothpaternal and maternal genomes contribute equallyin a developing zygote. However, a recent studysuggests that a large part of the paternal genomeis not expressed during early seed developmentand the maternal genome alone directs earlyembryogenesis.19 A plant heterozygous for theembryo lethal mutant gnom produces 25% abortedseeds indicating that the paternally derived GNOMgene (p-GNOM) is able to complement the maternalgnom (m-gnom) in the developing seed.20 However,a recent experiment indicates that when thedeveloping zygote is observed at a very early stage am-gnom/p-gnom seed and a m-gnom/p-GNOM seed lookidentical, both showing signs of impaired embryodevelopment, suggesting that p-GNOM is not active.19

However, at a later stage of embryo developmentthe m-gnom/p-GNOM becomes normal and producesnormal seed. In addition, by monitoring theexpression using a GUS reporter gene another 20paternally introduced loci were found not to beexpressed during early seed development suggestingthat many genes are silenced in Arabidopsis duringearly seed development.

Gametophytic control of fertilization

A female gametophytic mutation is clearly distin-guishable from a maternal effect mutation by itsgenetic behaviour. Self-pollinated heterozygousplants carrying a female gametophytic mutation

would produce 50% normal seed and 50% abortedseed. This genetic screen has been used to definea number of genes that give rise to gametophyticfemale sterility.21 In recent years a class of femalegametophytic mutations that has attracted widespread attention is the FIS class of genes ofArabidopsis that initiate Fertilization I ndependentSeed formation (reviewed in Reference 3).

Genetic screens designed to isolate mutants inwhom aspects of seed development are uncoupledfrom fertilization identified three genes, FIS1/MEA,FIS2 and FIS3/FIE. Two different genetic screens haveled to the isolation of alleles that define these threegenes.22–26 Two different allelic forms of FIS1, emb173and mea were also isolated as mutants that form50% shrivelled embryo arrested seed.22 All threemutations create the female gametophytic phenotypeof an arrested embryo following pollination andendosperm development without pollination.FIS1/MEDEA and FIS3/FIE encode members of thePolycomb group (PcG) proteins and FIS2 encodesa transcription factor with domains including a Znfinger, a unique domain with repeats, as well as a car-boxy terminal domain shared by a family of proteinin diverse organisms.1,26–28 FIS2 shares homology tothe Drosophila gene Su (z)12, a gene that controls theexpression of drosophila homeobox genes, and theArabidopsis genes EMF2 and VERN2, both involvedin flowering (reviewed in Reference 1). In addition itis partially homologous to a human gene KIAA1060in chromosome 17.1 It has been shown that FIS1 andFIS3 interact both in vitro and in vivo but no interac-tion of FIS2 has been shown with either FIS1 or FIS3.The precise mechanism of the interaction of FIS2with FIS1 and the FIS3 remains to be identified.3,29

The fis class of mutants also has an altered patternformation along the anterior–posterior axis of the de-veloping seed.30 When fis ovules are fertilized with FISpollen, chalazal cysts are producing not only in thechalazal region but also elsewhere and endospermmarkers normally expressed in the chalazal regionare also expressed in other endosperm domains.

In other species, PcG proteins form multiproteincomplexes that have a general repressive effect ongene expression, presumably through effects onchromatin remodelling.31 These genes are thoughtto be involved in establishing and maintaining anepigenetic state through successive cell division. Ithas been hypothesized that the FIS protein complexmight repress a number of target genes, some ofwhich are involved in controlling the initiation ofseed development.27

383


Figure 1. Parent specific expression of FIS2::GUS andthe rescue of the fis2 mutant seed by pollen from ahypomethylated plant. (A) Maternally derived FIS2:GUSactivity 24 h after pollination, (B) no GUS expression is seenwhen the same construct was introduced via pollination,(C) fis2/fis2 seeds rescued with pollen from C24 anti-MET1plant, (D) fis2/fis2 pollinated with C24 pollen showingshriveled seeds.

Parent of origin effect on seed developmentand DNA methylation

A paternally derived FIS allele is unable to rescue thematernal defect of maternal fis alleles. This result is

consistent with the idea of silencing of the paternallyderived FIS genes by imprinting.32 In support of thisidea the promoters of all three FIS genes linked toGUS reporter were found to be expressed maternallyin the developing endosperm and not expressedwhen derived paternally (Figure 1).32 It has beenpostulated that imprinting is mediated by DNAmethylation,33 and a gene DDM1 that controlschromatin remodelling has also been implicated incontrolling imprinting.34 Thus it is possible that analtered level of DNA methylation in the paternalgenome35 would change the parent of origin effectshown by the fis mutations. Using a transgenic DNAmethyltransferase 1 antisense (METI a/s) plant withreduced global levels of DNA methylation36 Luoet al.32 and Vinkenoog et al.37 demonstrated thatthe maternal defect of the fis mutations could berescued by reduced DNA methylation in the paternalgenome (Figure 1). However the rescue did notrequire the corresponding functional paternal allelesof MEA and FIS2 to be active.32 Paternally derivedMEA::GUS and FIS2:GUS still remained silencedduring early seed development even when they weredelivered from a hypomethylated pollen parent.Thus hypomethylation does not seem to breakthe imprinting of these two FIS genes nor are thefunctions of these genes required for mutant seedrescue.32 In contrast, for the rescue of the maternalfis3/fie allele by hypomethylated pollen there is anapparent need of a paternally derived FIE allele.37

These results indicate that important additionalgenes controlling imprinting and maternal effectremains to be identified.

Conclusions

Paternal and maternal genomes interact in a co-ordinated manner to produce seed. Evolutionaryarguments have been used to postulate a conflictof interest between the paternal and the maternalgenomes during seed development.38 Recentisolation of the FIS genes and the correspondingmolecular work involving parent of origin effect,imprinting, chromatin remodelling and DNAmethylation indicates that genetic as well asepigenetic processes mediate different aspects ofseed development. These studies begin an era ofintense molecular work that is likely to reveal anintricate regulatory network defining embryo andendosperm development.

In addition to illuminating an important area of

384


plant development these studies will help devisebetter strategies for food production in the world.39

References

1. Chaudhury A, Koltunow AM, Payne T, Tucker M, DennisES, Peacock WJ Early seed development. Ann Rev Cell DevBiol (in press)

2. Friedman WE (1998) The evolution of double fertilizationand endosperm: an “historical” perspective. Sex Plant Reprod11:6–16

3. Chaudhury AM, Craig S, Dennis ES, Peacock WJ (1998) Ovuleand embryo development, apomixis and fertilization. CurrOpin Plant Biol 1:26–31

4. Berger F (1999) Endosperm development. Curr Opin PlantBiol 2:28–32

5. Gasser CS, Broadhvest J, Hauser BA (1998) Genetic analysisof ovule development. Annu Rev Plant Phys Mol Biol 49:1–24

6. Baker SC, Robinson-Beers K, Villanueva JM, Gaiser JC, GasserCS (1997) Interactions among genes regulating ovule devel-opment in Arabidopsis thaliana. Genetics 145:1109–1124

7. Motamayor JC, Vezon D, Bajon C, Sauvanet A, GrandjeanO, Marchand M, Bechtold N, Pelletier G, Horlow C (2000)Switch (swi1), an Arabidopsis thaliana mutant affected in thefemale meiotic switch. Sexual Plant Reprod 12:209–218

8. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants.EMBO J 20:589–600

9. Felker FC, Peterson DM, Nelson OE (1985) Anatomyof immature grains of eight maternal effect shrunkenendosperm barley mutants. Am J Bot 72:248–256

10. Thompson RD, Hueros G, Becker HA, Maitz M (2001)Development and functions of seed transfer cells. Plant Sci160:775–783

11. Talierco EW, Kim JY, Mahe A, Shanker S, Choi J, Cheng WH,Prioul JL, Chourey PS (1999) J Plant Physiol 155:197–204

12. Hueros C, Gomez E, Cheikh N, Edwards J, Weldon M,Salamini F, Thompson RD (1999) Identification of apromoter sequence from the BETL1 gene cluster able toconfer transfer-cell-specific expression in transgenic maize.Plant Physiol 121:1143–1152

13. Maitz M, Santandrea G, Zhang ZY, Lal S, Hannah LC,Salamini F, Thompson RD (2000) rgf1, a mutation reducinggrain filling in maize through effects on basal endosperm andpedicel development. Plant J 23:29–42

14. Cheng WH, Taliercio EW, Chourey PS (1996) The Miniature1 seed locus of maize encodes a cell wall invertase requiredfor normal development of endosperm and maternal cells inthe pedicel. Plant Cell 8:971–983

15. Ray A, Lang JD, Golden T, Ray S (1996) SHORT IN-TEGUMENT (SIN1), a gene required for ovule developmentin Arabidopsis, also controls flowering time. Development122:2631–2638

16. Colombo L, Franken J, Van der Krol A, Witich P, Dons HJM,Angenent GC (1997) Downregulation of ovule-specific MADSbox genes from petunia results in maternally controlleddefects in seed development. Plant Cell 9:703–715

17. Ray S, Golden T, Ray A (1996) Maternal effects of theshort integument mutation on embryo development inArabidopsis. Dev Biol 180:365–369

18. Jacobsen SE, Running MP, Meyerowitz EM (1999) Disruptionof an RNA helicase/RNAse III gene in Arabidopsis causesunregulated cell division in floral meristems. Development126:5231–5242

19. Vielle-Calzada JP, Baskar, Grossniklaus U (2000) Delayedactivation of the paternal genome during seed development.Nature 404:91–94

20. Mayer U, Ruiz Rat, Berleth T, Misera S, Jurgens G (1991)Mutations affecting body organisation in the Arabidopsisembryo. Nature 353:402–407

21. Drews GN, Lee D, Christensen CA (1998) Genetic analysisof female gametophyte development and function. Plant Cell10:5–17

22. Grossniklaus U, Spillane C, Page DR, Kohler C (2001)Genomic imprinting and seed development: endosperm for-mation with and without sex. Curr Opin Plant Biol 4:21–27

23. Peacock WJ, Ming L, Craig S, Dennis E, Chaudhury A (1995)A mutagenesis programme for apomixis genes in Arabidopsis,in Induced Mutations and Molecular Techniques for CropImprovement, pp. 117–125. FAO/IAEA, Vienna, Austria

24. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, PeacockWJ (1997) Fertilisation-independent seed development inArabidopsis thaliana. Proc Natl Acad Sci USA 94:4223–4228

25. Ohad N, Margossian L, Hsu Y-C, Williams C, Repetti P, FischerRL (1996) A mutation that allows endosperm developmentwithout fertilisation. Proc Natl Acad Sci USA 93:5319–5324

26. Grossniklaus U, Vielle-Calzada JP, Hoepner MA, GaglianoWB (1998) Maternal control of embryogenesis by medea, aPolycomb group gene in Arabidopsis. Science 280:446–450

27. Luo M, Bilodeau P, Koltunow A, Dennis ES, PeacockWJ, Chaudhury AM (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. ProcNatl Acad Sci USA 96:296–301

28. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D,Haradr JJ, Goldberg RB, Fischer RL (1999) Mutations in FIE,a WD polycomb group gene, allow endosperm developmentwithout fertilisation. Plant Cell 11:407–416

29. Yadegari R, Kinoshita T, Lotan O, Cohen G, Katz A, Choi Y,Katz A, Nakashima K, Harada JJ, Goldberg RB, Fischer RL,Ohad N (2000) Mutations in the FIE and MEA genes thatencode interacting polycomb proteins cause parent-of-origineffects on seed development by distinct mechanisms. PlantCell 12:2367–2382

30. Sorensen MB, Chaudhury AM, Robert H, Bancharel E, BergerF (2001) Polycomb group genes control pattern formation inplant seed. Curr Biol 11:277–281

31. Pirrotta V (1998) Polycombing the genome: PcG, trxG, andchromatin silencing. Cell 93:333–336

32. Luo M, Bilodeau P, Dennis E, Peacock WJ, ChaudhuryAM (2000) Expression and parent-of-origin effects for FIS2,MEA and FIE in the endosperm and embryo of developingArabidopsis seeds. Proc Natl Acad Sci USA 97:10637–10642

33. Li E, Beard C, Jaenisch R (1993) Role for DNA methylation ingenomic imprinting. Nature 366:362–365

34. Vielle-Calzada JP, Thomas J, Spillane C, Coluccio A, Hoepp-ner MA, Grossniklaus U (1999) Maintenance of genomicimprinting at the Arabidopsis medea locus requires zygoticDDM1 activity. Genes Dev 13:2971–2982

35. Adams S, Vinkenoog R, Spielman M, Dickinson HG, ScottRJ (2000) Parent-of-origin effects on seed developmentin Arabidopsis thaliana require DNA methylation. Develop-ment 127:2493–2502

36. Finnegan EJ, Peacock WJ, Dennis E (1996) Reduced DNAmethylation in Arabidopsis thaliana results in abnormal plantdevelopment. Proc Natl Acad Sci USA 93:8449–8454

37. Vinkenoog R, Spielman M, Adams S, Fischer RL, DickinsonHG, Scott RJ (2000) Hypomethylation promotes autonomousendosperm development and rescues post fertilization lethal-ity in fie mutants. Plant Cell 12:2271–2282

385


38. Haig D, Westoby M (1989a) Parent specific gene-expressionand the triploid endosperm. Am Nat 134:147–155

39. Koltunow AM, Bicknell RA, Chaudhury AM (1995) Apomixis:

Molecular strategies for the generation of genetically identicalseeds without pollination. Plant Physiol 108:1345–1352

386

maternal control of seed development -...

Documents