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© 2000 Kluwer Academic Publishers. Printed in the Netherlands.
Genetic and epigenetic interactions in allopolyploid plants
Department of Botany, Box 355325, University of Washington, Seattle, WA 98195-5325, USA (e-mail: email@example.com)
Key words: chromosome evolution, gene silencing, heterochromatin, interspeciﬁc hybridization, recombination, transposons
Abstract Allopolyploid plants are hybrids that contain two copies of the genome from each parent. Whereas wild and cultivated allopolyploids are well adapted, man-made allopolyploids are typically unstable, displaying homeotic transformation and lethality as well as chromosomal rearrangements and changes in the number and distribution of repeated DNA sequences within heterochromatin. Large increases in the length of some chromosomes has been documented in allopolyploid hybrids and could be caused by the activation of dormant retrotransposons, as shown to be the case in marsupial hybrids. Synthetic (man-made) allotetraploids of Arabidopsis exhibit rapid changes in gene regulation, including gene silencing. These regulatory abnormalities could derive from ploidy changes and/or incompatible interactions between parental genomes, although comparison of auto- and allopolyploids suggests that intergenomic incompatibilities play the major role. Models to explain intergenomic incompatibilities incorporate both genetic and epigenetic mechanisms. In one model, the activation of heterochromatic transposons (McClintock’s genomic shock) may lead to widespread perturbation of gene expression, perhaps by a silencing interaction between activated transposons and euchromatic genes. Qualitatively similar responses, of lesser intensity, may occur in intraspeciﬁc hybrids. Therefore, insight into genome function gained from the study of allopolyploidy may be applicable to hybrids of any type and may even elucidate positive interactions, such as those responsible for hybrid vigor. Abbreviations: AFLP-cDNA, ampliﬁed fragment length polymorphism of copy DNA; HDGS, homologydependent gene silencing; LTR, long terminal repeat; RFLP, restriction fragment length polymorphism; RT-PCR, reverse transcriptase polymerase chain reaction; WU-BLASTN, Washington University Basic Local Alignment Search Tool, nucleotide comparison algorithm.
Introduction Whereas wild and cultivated allopolyploid plants are well adapted, man-made allopolyploids are typically unstable. Instability refers to the appearance of unexpected changes in phenotype, such as homeotic transformation and lethality, and in genome structure, such as chromosomal rearrangements and changes in the number and distribution of repeated DNA sequences within heterochromatin. These instabilities are presumably eliminated by evolutionary adaptations giving rise to stable species. However, the molecular
mechanisms underlying these adaptive steps remain obscure. This review provides examples of instability and considers the genetic and epigenetic mechanisms that may be responsible for instability. Interspeciﬁc hybrids between distant relatives are usually sterile. In 1912, Digby found a fertile plant that appeared spontaneously among the sterile hybrids generated in a cross between two primrose species; this plant had twice the number of chromosomes of its sterile sibs (Digby, 1912). While the signiﬁcance of chromosome doubling eluded Digby, Winge, unaware of Digby’s results, speculated that speciation could
[ 267 ]
. The two parental genomes in an allopolyploid. generating progeny with numerous combinations of parental chromosomal segments which can then be ﬁxed by selection (Ungerer et al. 1998). Genomic instability and restructuring The genomes of established allopolyploids can be changed considerably from the parental genomes (Kamm et al. Zhao et al. 1995. or after zygote formation (Ramsey and Schemske. 1995. and by Karpechenko (1927) in radish and cabbage. while pairing and recombination between homeologous chromosomes hinder the normal progress of meiosis by forming. B. 1976... 1999). are quite common in nature (Soltis and Soltis. for example.. Wendel et al. diploid hybrids freely recombine the two parental genomes. Feldman et al. Nevertheless. 1993. Rieseberg and Noyes. In contrast. Allopolyploids represent a special type of hybrid. 1998). studies with synthetic (man-made) allopolypoids suggest that the observed genomic changes occurred in a burst after allopolyploidization (Song et al. Therefore. Homeologous recombination Homeologous recombination is generally deleterious. conclusions about genomic alteration were based on the structure of parental genomes inferred from the structure of the presumed diploid descendants. Karyotypic divergence between species prevents normal meiotic pairing of chromosomes at metaphase I in the diploid hybrid. 1995. Leitch and Bennett.. Chiasmata between paired parental chromosomes in a diploid hybrid allow the combination of advantageous parental genome segments while both parental genomes remain ﬁxed in the allotetraploid hybrid. Volkov et al. He reasoned that upon doubling.. karyotypic stability is achieved at the expense of the evolutionary ﬂexibility provided by unhindered recombination between the parental genomes.. called homeologous. their widespread distribution implies that allopolyploidy is often advantageous. during meiosis (forming 2N gametes). while genome duplication in the allotetraploid hybrid allows normal pairing. Jiang et al. 1993. Winge believed that hybrid sterility was caused by unbalanced chromosome sets. 1997. Production of an allotetraploid hybrid requires a genome duplication step (GD).. Allopolyploidy hinders recombination between parental genomes. One factor that favors allopolyploids may be heterosis generated by the combination of homeologous genes (Allard et al. hybrid species that contain two or more diploid sets of parental genomes. Yet. 1998. Another factor may be the instability of new allopolyploids which.. The parental origin of chromosomes is marked by black and white. This prediction was experimentally veriﬁed by Clausen and Goodspeed (1925) in tobacco species. The forced maintenance of two integral parental genomes should limit the evolutionary ﬂexibility of allopolyploid hybrids. 1998).388 Figure 1. Comparison of diploid and allotetraploid hybrids. 1998). A. 1998). undergo little intergenomic recombination and thus maintain their integrity through sexual generations (Figure 1B). Since the original parents were not available. a proper pairing partner would be available to each chromosome resulting in fertility (Figure 1A). trivalents [ 268 ] . Perfect homologous pairing in allotetraploids is often a secondary adaptation (Sears. Moore. 1917). Two mechanisms that could cause these genomic changes are recombination and transposon activation. 1998). although usually deleterious.. might generate sufﬁcient phenotypic variation for the exploitation of new ecological niches. Recombination between repeated regions destabilizes the genome by producing deletions and chromosomal rearrangements. It was soon realized that allopolyploids. occur by interspeciﬁc hybridization followed by chromosome doubling (Winge. 1997. Liu et al. which can occur in the parents (forming autopolyploids).
DNA mismatch repair is initiated when a mutS-like protein binds to a mismatched base pair or displaced loop in double-stranded DNA (Modrich and Lahue. it rejects recombination partners when it senses mismatches in recombination-generated heteroduplexes (Figure 3B). In some AB allotetraploids..389 system has at least two functions: in addition to repairing mismatches produced during replication. Additionaly. 1989). For example. Kolodner and Marsischky.. 1995). However. Humbert et al. Alternatively. Furthermore. three genera with basic diploid genomes (A. even though DNA can be exchanged by conjugation. 1998) and homeologous recombination (Bailis and Rothstein. bacteria deﬁcient in mismatch repair underwent frequent deletion of DNA ﬂanked by homeologous direct repeats (Petit et al. this may cause a further increase in homeologous recombination (see below). 1998. This peculiar coincidence could be explained by assuming that an ancestral progenitor of the Brassica species had direct repeats in that region of the genome. a case of genomic instability in a synthetic Brassica allopolyploid might be explained as a case of homeologous recombination (Song et al. 1995. Wild-type Salmonella typhimurium is unable to recombine its DNA with that of Escherichia coli... The occurrence of homeologous recombination depends on the history of allopolyploids.. In this study.. recombination between the homeologous parental genomes can be frequent and may contribute to genome restructuring. whose concentration is usually low. which maintained the two re- Figure 2. 1991). Such an event did not occur in the parental B genome. b). coli (Rayssiguier et al. Salmonella mutants deﬁcient in mismatch repair were capable of conjugational recombination with E. As a consequence. 1998. failure of mismatch repair increases both the mutation rate (Fishel and Kolodner. corresponding to homologous and homeologous pairing respectively. Chambers et al. forcing the establishment of a diploid-like meiosis in which the chromosomes of each parental set pair only with their homologues. such as wheat Ph1. On the other hand. and univalents (Figure 2). In newly formed allopolyploids. Mechanisms acting at different levels of chromosome pairing have been postulated (Moore. Vega and Feldman. 1995. 1996). 1983. 1996). smallerthan-expected restriction fragment. can also suppress homeologous pairing (Sears. Prolla. mismatch repair proteins. 1998a. 1997.. 1999). 1998). Collapse of mismatch repair would induce genomic instability in a manner consistent with observations made in allopolyploids (Figure 4). 1996. allowing recombination only when it recognizes a certain threshold of similarity (Luo et al. 1976). Mikhailova et al. The mismatch repair [ 269 ] . homeologous recombination is rare in established allopolyploids. After speciation of the C genome. These new RFLPs were not found in the parental A and B genomes. The nature of Ph1 is unknown. Chromosome pairing in allotetraploids. 1990. B. they were identical in size to the RFLP found in the C genome. In a positive feedback loop.. however. can be titrated by an excess of mismatches during incipient recombination between homeologous genomes (Claverys et al.. genetic analysis suggests that certain genes. probes used for restriction fragment length polymorphism (RFLP) mapping hybridized to a new. with grave consequences for the function and integrity of the genome. C) were hybridized in pairwise combinations. a recombination event between the repeats deleted the intervening DNA. Normal (left) and aberrant (right) metaphase I ﬁgures. leading to replacement of a large patch of single-stranded DNA containing the mismatch (Figure 3A). The function of mismatch repair could thus be compromised in interspeciﬁc crosses. Hunter et al. 1996. Selva et al. Furthermore. It is possible that higher expression levels of mismatch repair proteins would be required for stability of allopolyploids than autoploids. 1995). Jiricny. Homeologous recombination in recently formed allopolyploids may play a role in their instability. a related bacterium about 80% similar in DNA sequence.. The destabilizing effect of homeologous recombination might be better understood by considering its relationship to post-replicative DNA mismatch repair.. Ph1 could control chromosomal movement or condensation or could recognize chromosomal features other than DNA sequence (Aragon-Alcaide et al. Ph1 could encode a ‘local editor’ that screens pairing partners on a DNA segment by segment basis. Progressive differentiation of the parental genomes in allopolyploids may prevent homeologous synapsis and recombination.
[ 270 ] . suggesting that hybridization ‘initiated mobilities of these elements’. and encompass retroelements. A. mutS protein could be depleted. DNA mismatch repair in eukaryotes is initiated by the binding of a mutS-homologue dimer to the mismatch and proceeds to excision and resynthesis of the mismatched DNA strand. Selva et al. a decrease in mismatch repair function might have allowed the two homeologous repeats to undergo the same recombination event. Normally. resulting in a deletion and formation of the C-speciﬁc RFLP. The black and gray arrows represent homeologous sequences. it is consistent with two phenomena observed in allopolyploids: meiotic drive and chromosome expansion. Production of a smaller restriction fragment by deletion of a region ﬂanked by homeologous direct repeats (arrows). 1984).. A. It is common in newly synthesized allopolyploids as well as in diploid hybrids and is associated with heterochroFigure 4. 1995). allowing homeologous DNA strands to continue the recombination process (Humbert et al. binding of mismatch repair proteins to the mismatches blocks recombination (Rayssiguier et al. Because of junction movement (branch migration) complementary homeologous strands form heteroduplexes that contain mismatches (small arrows). and related heterochromatic repeats. Transposon activation Barbara McClintock believed that genomic incompatibilities unmasked by interspeciﬁc hybridization are among the causes of genomic shock.. peats.390 Figure 3. B. A possible role for DNA mismatch repair in allopolyploidy. a programmed response to stress (McClintock. Bailis and Rothstein. 1996). Circles represent centromeres. B.. Meiotic drive Meiotic drive refers to the subversion of meiosis by a locus that causes its own preferential segregation. Chambers et al. 1989.. A Holliday junction is formed by recombination between two homeologous chromosomes. Upon AB allopolyploidization. If an excessive number of mismatches are formed. 1990. She pointed to the difference in repetitive elements between the two parental genomes as a cause of genomic shock. 1995. Although this hypothesis has not been directly tested. Two examples of genomic changes caused by homeologous recombination. Genomic consequences of recombination between homeologous DNAs. Formation of an acentric and a dicentric chromosome. The terms ‘repetitive elements’ and ‘transposons’ are used intercheangeably in this review. The ladder represents dsDNA. DNA transposons.
1994.) that had been transferred by recombination to a Nicotiana tabacum (N. Liu et al. polymorphic heterochromatic regions that are detectable cytologically in various chromosomal positions (Buckler et al. The images are from microphotographs of Gerstel and Burns (1967). because larger knobs result in higher degrees of preferential segregation. In some cells the abnormal chromosomes Figure 5..391 matin and chromosomal breaks.. The knobs are activated to ‘drive’ by the presence of a large heterochromatic region. 1967). In these marsupials. While these studies on chromosome expansion in Nicotiana predated modern molecular analysis. abnormal chromosomes. of Nicotiana otophora (N. B... In maize. Normal chromosomes (some of the largest in the normal karyotype). The Ab10 interaction with the knob heterochromatin exempliﬁes how the relationship between controlling loci and a family of heterochromatic repeats may contribute to the restructuring of allopolyploid genomes. and megachromosomes are shown to the same scale. Pollen killer genes are a probable cause of the frequent sterility observed in synthetic allopolyploids. higher numbers are incompatible with survival of the hybrid species bearing them. Indirect evidence for activation of dormant transposons comes from a study of hybridization between Nicotiana otophora and N.. A. 1997. drive their inheritance by causing chromosomal breaks in meiotic products in which they are absent (Endo. Instability was evident as chromosome breakage as well as heterochomatin expansion at the knob site (Figure 5). 1998) might depend on the relationship of these repeats to transposable elements (Flavell et al. presumably a knob.t. Expansion of chromosomes in Nicotiana allopolyploids. Expansion of chromosomes The frequent changes in copy number and chromosomal position of repeats (Feldman et al. suggesting that the formation of the megachromosomes occurred in a single cell division cycle and that their presence blocked further cell divisions. 1967).o. 1998). the knobby arm of abnormal chromosome 10 (Ab10). 1998). While one or two pollen killer genes can be tolerated. 1942).) chromosome. Jurka. 1997). Gerstel and Burns. the inactivated X-chromosome of female mammalian cells. In the presence of Ab10. The progressive expansion of two normal chromosomes to ‘abnormal’ and ‘mega’ length was attributed to a single heterochromatic region. loci involved in meiotic drive coincide with knobs. 1990). A well studied instance of meiotic drive was discovered in crosses between North American and Latin American maize lines (Rhoades. for example. Megachromosomecontaining cells were always surrounded by cells with the simple ‘abnormal’ chromosomes. an ancient tetraploid (Whitkus et al. Although the molecular basis of this phenomenon is unclear. This indicated that the additional DNA in these chromosomes was packaged as heterochromatin.to 30-fold to become ‘megachromosomes’! Cells that harbored either the abnormal chromosomes or the megachromosomes exhibited condensed chromatin regions in interphase nuclei that resembled a Barr body. [ 271 ] . they bear a striking similarity to those made in wallabie hybrids (O’Neill et al. each knob assumes neocentromeric activity and is preferentially inherited during megasporogenesis (Yu et al. the chromosome-breaking action is reminiscent of that of transposons and may account for at least part of the extensive genome restructuring in allopolyploids. In conclusion. Knob expansion could double the size of the affected ‘abnormal’ chromosomes.. 1999). Furthermore. Pollen ‘killer’ genes. underwent an even more dramatic change: they increased their length by 20. tabacum in which an otophora chromosome segment containing a heterochromatic knob and a ﬂower color gene became spontaneously unstable (Burns and Gerstel. 1992). 1967.. these rarely cited studies document a remarkable case of heterochromatin expansion and instability in allopolyploid hybrids. Chromosome expansion was accompanied by ﬂower color variegation induced by chromosomes breakage followed by loss of the heterochromatic block and of the knob-distal Cov gene (Burns and Gerstel. the Ab10 meiotic drive system may favor expansion of the heterochromatic repeats that comprise the knobs.
.. 1970). 1996). Gutierrez et al. An alternative approach that samples more genes is the comparative mutagenesis of an allopolyploid and its diploid parents. Recessive nulli.. Allopolyploids that survive are usually vigorous. they should be inactivated by mutations (Ohno. van Buuren et al. wheras silencing refers to loss of gene activity by epigenetic changes (see below).. inactivation of the redundant genes would be taken to be 100% (implying no gene redundancy in the allopolyploid). 1995. Cronn et al. implying a lack of orthologous function in a homeologous gene. D’Hont et al. but sparsely investigated phenotypic symptoms of instability are sterility and lethality.or hypomorphic mutations affecting phenotype can only occur at non-redundant loci.. 1994.. Henikoff and Comai. Gene inactivation is used here to deﬁne loss of gene activity by genetic changes. 1993. the high induced-mutation rate may have an epigenetic base. If the types of genes sampled by induced mutagenesis are representative of all genes. 1990). 1983. depending on the particular gene (Guo et al. 1994. Perhaps the most dramatic. In maize.. was associated with a sharp decline of cytosine DNA methylation (discussed below). hybridization of Nicotiana allopolyploids may have reactivated dormant transposons. Pichersky et al. By scoring embryo lethal mutations representing about 500 loci (Meinke. In Arabidopsis. Small et al. 1999). Therefore.. Boisselier Dubayle et al. The ratio of the induced mutation rate for the allopolyploid to the rate for its parents can be used to measure gene inactivation at the sampled loci. O’Kane et al. In crosses between Nicotiana species extensive lethality is also seen at the seedling stage (Marubashi et al. 1967). 1994. 1991. A. First. 1956) and cotton (Meyer. while demonstrable in some cases. 1999. the ploidy level can either increase or decrease expression. missense mutations could not alter transcription of the affected gene. For example. Burns and Gerstel. 1996).392 chromosome expansion was caused by the runaway replication of a retrotransposon which. 1999). Rieseberg and Soltis. or by DNA sequencing. I observed similar rates of induced mutations in the allotetraploid Arabidopsis suecica (unpublished results). 1998a. Song and Osborn.. 1994). yet they do show some unusual characteristics such as homeotic phenotypes in Digitalis (Schwanitz. Much less is known about the effects of allopolyploidy Phenotypic and molecular alterations Gene inactivation The redundancy of genetic information in polyploids implies that unless duplicated loci gain a useful function. a natural hybrid of [ 272 ] . and the suppression of certain G1 cyclins is thought to be responsible for the increase in cell size that accompanies polyploidy (Galitski et al. Gastony. 1997). which are manifested phenotypically but without changes in DNA sequence (Jacobsen and Meyerowitz. 1999). usually during embryonic development.. a case of transgene silencing is correlated with tetraploidy (Mittelsten Scheid et al. 1996. 1958). is relatively infrequent (Hart. The results suggest that inactivation. and dominance of the hybrid phenotype by one parent in triticale (Heslop-Harrison. Therefore.. Soltis and Soltis. Second. Hanfstingl et al. 1999).. The frequency of mutations that reduce or abolish chlorophyll accumulation in diploid and allotetraploid wheat suggested that 20% of the duplicate genes in the allotetraploid were inactivated (Stadler.. 1990. 1989. in yeast expression of several genes is affected by ploidy level. 1929. 1994. resulting from the formation of epialleles. 1996. Mac Key. in turn. the level of genetic inactivation inferred from mutagenesis experiments appears higher than one might expect from experiments that monitored the expression or structure of sampled homeologous genes (see above). thaliana and Cardaminopsis arenosa (Kamm et al. 1989. Polyploidy alone can affect the expression of certain genes. 1954. Odrzykoski et al. inactivation may stem from alterations not detected by the assay used. 1992. There are two possible explanations that may reconcile these data. Most synthetic allopolyploids display poor development and reduced survival of gametophytes and following fertilization. high lethality among the zygotes. ﬂower variegation and tumor formation in Nicotiana (Kehr and Smith. 1996). Vaucheret et al. For example. What fraction of the genes is inactivated in natural allopolyploids? Most work relevant to inactivation involved selected genes that were studied by isozyme or mRNA analyses.. if allopolyploid and parents show the same induced mutation rate. 1957).. Analysis of gene expression in synthetic allopolyploids In synthetic allopolyploid hybrids genomic restructuring and unstable phenotypes could stem from alterations in gene regulation (Matzke et al.. 1970).. Gilia (Grant.
thaliana are relatively stable and fertile (Scott et al.. homeotic phenotypes and tumors suggesting that certain genes regulating development were malfunctioning. from demethylation. showed otherwise. thaliana should facilitate the molecular analysis of gene regulation in allopolyploids. but not differences in ploidy (Galitski et al. The abnormal phenotypes included dwarﬁsm.. thaliana and C. suecica. Gish. embryo lethality and great variability in many morphological features. Thus. they indicate that rapid gene silencing occurs in synthetic allopolyploids and point to a relationship between the silenced genes and repetitive DNA of presumed heterochromatic origin. These results suggest that a thorough comparison of gene regulation in allopolyploids and their parents should help in understanding the consequences of hybridization on genomic function. For example. the increased rate of abnormalities upon demethylation suggests that this phenotypic instability resulted. 1983. however. WU-BLASTN similarity analyses (W. arenosa rRNA [ 273 ] . we synthesized allotetraploid hybrids of A. The genomic resources available in A.. we investigated the effect of 5-aza-2 -deoxycytidine (azaC). Guo et al. In addition to displaying frequent sterility. control synthetic hybrids displayed the usual variability but failed to show the high frequency and intensity of aberrant phenotypes displayed by the azaC-treated cohort. aberrant branching patterns. displays silencing of the A. the repetitive element was determined to be a ‘solo’ long terminal repeat.wustl. suecica. Investigation of nucleolar dominance in the same synthetic hybrids that were used for gene silencing studies (see above) revealed that the F1 hybrids differed from one another in rRNA gene expression. Furthermore. thaliana and 16 from C. of certain DNA sequences. A. 1996).. 1998). directly or indirectly. We employed AFLP-cDNA analysis. http://blast. tetraploid and pentaploid hybrids in Nicotiana all form genetic tumors with comparable frequency (Kehr and Smith..edu) and Southern blotting revealed that these three genes contain repetitive DNA. a PCR-based method that displays random restriction enzyme fragments of cDNA on denaturing polyacrylamide gels (Bachem et al. Bender and Fink. Therefore. the synthetic hybrids produced abnormal phenotypes at high frequency (Comai. some hybrids (5 to 80% depending on the trait) displayed unusual phenotypes including homeotic aberrations and chimeric ﬂower morphology. Interestingly. 2000). we used lines with the same ploidy: the parents were autotetraploid and the progeny were allotetraploid. We compared gene expression in the hybrids and in the parents. thaliana ecotypes treated with azaC grew normally. an LTR found alone and not ﬂanking an intact retrotransposon (Wirth et al. 1960). Furthermore. allopolyploidy may have an even greater effect on gene regulation. they appear more stable than synthetic allopolyploids (Allard. showing variation between co-dominance and dominance of the C. Effect of DNA cytosine demethylation To further explore the link between instability in allotetraploids and cytosine DNA methylation. arenosa.. although they were present in the parents and in a mixture of parental mRNAs. fasciation. 1999. and by molecular marker analysis (Comai et al. arenosa. comparison of cytosine methylation in these families of LTRs by HpaII and MspI restriction digestion revealed strong CG methylation in both hybrids and parents.. spontaneous and induced autopolyploids of A. Since azaC derepresses silenced genes (Hepburn et al. an inhibitor of cytosine DNA methylases. and perhaps derepression. 2000). 1996–1999. 1983). The synthetic allotetraploids had diploid sets of the parental genomes as indicated by the presence of 26 chromosomes. one might expect that azaCtreated synthetic allopolyploids would show fewer abnormalities. whereas synthetic allotetraploids are unstable and show poor fertility (Comai et al. probably because the incompatibilities between different genomes are more disruptive than changes caused by additional copies of the same genome. unpublished observations). triploid. diploid. In contrast.393 on gene regulation. Thus. These results show that the synthetic hybrids were phenotypically hypersensitive to demethylation. By RT-PCR analyses we conﬁrmed silencing of three genes out of about 20 silencing candidate genes examined. The results. 1995). The analyses revealed several products that were absent in the F2 hybrids. 1954). 10 from A. To identify changes due to allopolyploidization. Whereas tetraploid parents and ﬁve diploid A. which are the synthetic counterpart of the natural allotetraploid A. 1996).. Nucleolar dominance Nucleolar dominance refers to the silencing in hybrids of one parental set of rRNA genes. but decreased methylation at CNG sites in the hybrids. thaliana rRNA genes. In one case. the natural allopolyploid. Whereas synthetic autopolyploids are less stable than the corresponding diploids.
they are deleterious in a hybrid genetic background due to the accumulation of incompatible features since divergence of the two taxa. 1967). and the variable hybrid phenotype (Comai. arenosa rRNA genes. interactive components of a system evolve as a coordinated set. Epigenetic model Epigenetics refers to heritable changes in phenotype. 2000). 1999). which requires methylation (Jeddeloh et al. 1998). thaliana genes and dominance of the C. while certain genes are neutral or advantageous in their species of origin. This instability was resolved in the F2 plants which consistently showed silencing of the A. arenosa. however. 1970. Comai.. One epigenetic phenomenon. Schwanitz. Epigenetic interactions in the hybrids may occur between homeologous genes or between genes and related sequences within heterochromatin. Deﬁciency in the maintenance of DNA methylation could have severe consequences such as the derepression of dormant tranposons (see below). 1998. respectively). Similarly. 1991). For example. and hence in gene regulation. As a result of these constraints. Wolffe and Matzke. poorly matched components would be forced to interact and may function aberrantly. an epigenetic interaction between the ribosomal RNA genes of the two parents may determine the outcome. The abnormal phenotypes of the allopolyploids are better explained as being caused by epigenetic changes than by mutation (Grant. can be proposed to explain instability and silencing. Two general models. Meyer. In the hybrid. such as the maintenance and remodeling of chromatin states. Upon speciation. and it is reviewed elsewhere in this issue. 1999).. 2000). According to Dobzhansky. orthologous sets may diverge from each other as exempliﬁed in Figure 6. involves the suppression of one gene by another homologous gene (Wolffe and Matzke. 2000). be reversed by changing the parental genomic ratio from 1:1 (AACC) to 3:1 (AAAC. Taken together these observations indicate that allopolyploid formation may be associated with epigenetic changes. Mechanisms generating instabilities in synthetic allopolyploids Genome instability and gene silencing in allopolyploids may stem from impairment of mechanisms regulating important genomic functions. This dominance relationship could. Genes that were rapidly silenced upon allopolyploidization were related to repetitive DNA elements (Comai.394 protein or by interacting proteins.. Both models extend a proposal by Dobzhansky (1937) to explain hybrid inviability. Assembly of a defective heteromeric protein complex in a hybrid. thaliana and C. homology-dependent gene silencing (HDGS). What features of the genomic and phenotypic instabilities of synthetic allopolyploids implicate epigenetic phenomena? Some genomic alterations suggest the derepression of transposons that were dormant in the parents (Gerstel and Burns. even slight alterations in the structure of the protein subunits of complexes involved in chromatin regulation should result in altered function. The events predicted by the models could occur sequentially or independently. genes (Chen et al. one genetic and the other epigenetic. The allopolyploids were phenotypically hypersensitive to genome demethylation suggesting a relationship between chromatin suppression of genes. Subunits of a protein complex vary slightly between species. A and C represent the haploid genome of A. Epigenetic interactions between homeologous genes Genes that have silencing properties are usually associated with repeats: a type of silencing called paramu- Figure 6. that are not caused by changes in DNA sequence. 1956. Upon hybridization. a complex assembled from incompatible subunits may function irregularly or not at all. Instead. expression of a diverged mutS allele caused failure of mismatch repair in bacteria (Prudhomme et al. 1957. Genetic model This model of instability is based upon the mutual evolutionary constraint exerted by subunits of the same [ 274 ] . a common characteristic of genes susceptible to HDGS. Stochastic onset of nucleolar dominance and a reversal of the direction by chromosomal dosage are difﬁcult to explain with the normal rules of genetics.
Matzke and Matzke. the joining of homeologous genomes might bring together genes that undergo silencing interactions. 1994. insight into genome function gained from the study of allopolyploidy may be applicable to hybrids of any type and may even elucidate positive interactions. 1998b). The research [ 275 ] . Unusual phenotypes may be readily observed in allopolyploids because they produce viable progeny whereas diploid hybrids between distantly related parents are sterile. Speciﬁcally. Qualitatively similar responses. 1999). 1984). genes that have received transposon sequences that confer new regulatory properties (Wessler et al. SUPERMAN. However. homeologous genes sequestered in different diploid species should be free to diverge and accumulate characteristics that would emerge as incompatible when the homeologous genes are united by hybridization (Henikoff and Comai. all sequences similar to those of the inducing transcripts would be targeted. 1966. Martienssen. of lesser intensity. 1996. Hollick et al. 1997. 1999). while demethylation of the transposon decreases expression of the gene (Martienssen. such as those responsible for hybrid vigor.. Therefore.. epigenetic interactions between the parental genomes are likely to inﬂuence the outcome of this type of hybridization by affecting both genome structure and function. 1997).. 1998a).. The resulting trauma (McClintock’s genomic shock) may lead to widespread perturbation of gene expression. which was hypermethylated in its promoter region as if targeted by HDGS (Jacobsen and Meyerowitz. Within a species. Acknowledgments I would like to thank Arnold Bendich and Renata Fava-Ditt for suggestions and comments. Thus. 1996). 1998b). The phenotypic susceptibility of allopolyploid hybrids. Ronemus et al. 1998b. to the demethylating agent azaC might originate from a reduced ability of the hybrids to maintain suppressive chromatin complexes (see Figure 7B). Flavell. The proposed silencing interaction between derepressed repeats and euchromatic genes provides an explanation for the mysterious homeotic phenotypes caused by genome-wide demethylation in Arabidopsis (Finnegan et al. Thus. I suggest that it is the plant defense response against activated heterochromatic transposons that is responsible for silencing euchromatic genes that contain transposon-like sequences (Figure 7A). Epigenetic interactions between a gene and related heterochromatic repeats Interference of transposons with the regulation of euchromatic genes was ﬁrst described by McClintock (1965).. Baulcombe. The effect of a transposon insertion within a gene is not always predictable. It is possible that the loss of methylation derepressed heterochromatic transposons containing sequences similar to those within the SUP gene promoter. may occur in intraspeciﬁc hybrids. 1998a.395 tation results from the interaction of incompatible alleles which often contain transposon-related sequences and repeats (Brink et al. Bestor. 1995) should be highly sensitive to suppressive methylation of the transposonderived regulatory element. initiating the events modeled in Figure 7A. the frequent presence of transposons near euchromatic genes has spawned the theory that gene silencing is the effect of an epigenetic mechanism to suppress transposons (Martienssen. 1998a. methylation of a transcriptional regulatory region is likely to suppress transcription (Wolffe and Matzke. 1990. but not their parents. Instead. As a result. selection should act to avoid allelic divergences that raise the silencing potential beyond a tolerable threshold. Matzke and Matzke. the suppression of transposons that constitute a large fraction of plant genomes may be compromised in recent allopolyploids. 1968. Conclusion Conventional genetic rules alone are inadequate to explain the instability of allopolyploids. Since the suggestion that HDGS arose as a mechanism to silence transposons (and viruses) has gained acceptance (Matzke et al. Once HDGS has been triggered by elevated expression of transposons. Extending McClintock’s proposal that transposons may become activated in newly formed allopolyploids (McClintock. the epigenetic interactions triggered by hybridization in allopolyploids would not be fundamentally different from those occurring in diploid hybrids. perhaps by a silencing interaction between activated transposons and euchromatic genes. In certain cases methylation of the transposon favors expression of that gene (by blocking production of transposon transcripts that interfere with the normal gene transcript). Wolffe and Matzke. On the other hand. One such phenotype was caused by a silenced gene. 1999)..
S. 485 pp. T.. 1999. post-transcriptional silencing could also be involved.E. 1996. in my laboratory on gene regulation in allopolyploids is supported by USDA-NRICGP Grant 9901352. and Perez de la Vega. expression of the repeats triggers a genome defense that leads to silencing of the repeats. and Rothstein. Reader. or enhancer. 1990. P. but not by azaC treatement (Comai. Model to explain the hypersensitivity of Arabidopsis allopolyploids to 5-aza-2 -deoxycytidine (azaC) and the resistance of the parents. Virol. Suppl. 1996. Saenz-de-Miera. 15: 189–201. Viruses and gene silencing in plants. Allard. at times. R. and Moore. M. whose repeats are completely suppressed.W. cause complete derepression as illustrated in A. L.396 Figure 7. I. II. or transcribed region. Kakutani et al. Note that allopolyplody may. AzaC treatment would result in complete derepression in the hybrids. The gene sequence similar to the repeats could be located in the gene promoter. C. R. the production in diploid Arabidopsis of homeotic phenotypes upon suppression of methylation by genetic means (Finnegan et al. Plant J. A. Evolution of multilocus genetic structure in Avena hirtula and Avena barbata. References Allard. whose repeats are postulated to be already partially derepressed. 9: 745–753. New York. possibly. Allopolyploidization and azaC treatment are hypothesized to be incrementally effective in derepressing heterochromatic repeats. B.. 1993. but not in the parents. A. Wiley... Arch. [ 276 ] . Although the illustration depicts a case of transcriptional silencing by repressive chromatin. 1997. suggests that the latter methods are more effective than azaC treatment. D.B. A defect in mismatch repair in Saccharomyces cerevisiae stimulates ectopic recombination between homeologous genes by an excision repair dependent process. Miller. Genetics 126: 535–547. Ronemus et al. III.W. unpublished results).. 1996). Centromeric behaviour in wheat with high and low homoeologous chromosomal pairing.. a well expressed gene contains a sequence similar to that found in repressed heterochromatic repeats.W. Principles of Plant Breeding. G. but also to silencing of the cognate gene. Bailis.M. R. Chromosoma 106: 327–333. Aragon-Alcaide. Model for silencing of genes by activated heterochromatic repeats. the repeats are activated by a genomic shock leading to production of RNA (and. Additionally. Baulcombe. Genetics 135: 1125–1139. Visualization of differential gene expression using a novel method of RNA ﬁngerprinting based on AFLP: analysis of gene expression during potato tuber development. 1996. L. Garcia. 1960. Bachem. et al. transposition)..
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