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分子生物学

REVIEW/SYNTHE`SE

Size matters in Triticeae polyploids:larger genomes have higher remodeling

Miguel Bento,J.Perry Gustafson,Wanda Viegas,and Manuela Silva

Abstract:Polyploidization is one of the major driving forces in plant evolution and is extremely relevant to speciation and diversity creation.Polyploidization leads to a myriad of genetic and epigenetic alterations that ultimately generate plants and species with increased genome plasticity.Polyploids are the result of the fusion of two or more genomes into the same nu-cleus and can be classified as allopolyploids(different genomes)or autopolyploids(same genome).Triticeae synthetic allopo-lyploid species are excellent models to study polyploids evolution,particularly the wheat–rye hybrid triticale,which includes various ploidy levels and genome combinations.In this review,we reanalyze data concerning genomic analysis of octoploid and hexaploid triticale and different synthetic wheat hybrids,in comparison with other polyploid species.This analysis reveals high levels of genomic restructuring events in triticale and wheat hybrids,namely major parental band disappearance and the appearance of novel bands.Furthermore,the data shows that restructuring depends on parental genomes,ploidy level,and se-quence type(repetitive,low copy,and(or)coding);is markedly different after wide hybridization or genome doubling;and affects preferentially the larger parental genome.The shared role of genetic and epigenetic modifications in parental genome size homogenization,diploidization establishment,and stabilization of polyploid species is discussed.

Key words:genome restructuring,Triticeae,synthetic hybrids,polyploids.

Re′sume′:La polyplo?¨disation est l’une des forces motrices les plus importantes de l’e′volution chez les plantes et joue un ro?le important dans la spe′ciation et la cre′ation de diversite′.Elle me`ne a`un ensemble d’alte′rations ge′ne′tiques et e′pige′ne′ti-ques qui ge′ne`rent ultimement des plantes et des espe`ces avec une plasticite′ge′nomique accrue.Les polyplo?¨des re′sultent de la fusion de deux ge′nomes ou plus au sein d’un me?me noyau et sont classifie′s en allopolyplo?¨des(des ge′nomes diffe′-rents)et autopolyplo?¨des(le me?me ge′nome).Les allopolyplo?¨des synthe′tiques chez les Tritice′es constituent d’excellents mode`les pour e′tudier l’e′volution des polyplo?¨des.Cela est particulie`rement le cas pour le triticale,un hybride entre le ble′et le seigle,lequel pre′sente divers niveaux de plo?¨die et combinaisons ge′nomiques.Dans cette synthe`se,les auteurs re′exa-minent les donne′es portant sur l’analyse ge′nomique de triticales hexaplo?¨des et octoplo?¨des,ainsi que diffe′rents ble′s hybri-des synthe′tiques,en les comparant a`d’autres espe`ces polyplo?¨des.Cette analyse re′ve`le d’importants changements dans la structure des ge′nomes chez le triticale et les ble′s hybrides dont:la disparition de bandes parentales majeures et l’appa-rition de nouvelles bandes.De plus,les donne′es montrent que ces re′arrangements structuraux de′pendent des ge′nomes pa-rentaux,du niveau de plo?¨die et du type de se′quence(re′pe′titive,a`faible nombre de copies et codante/non-codante).Ils diffe`rent de fac?on importante selon qu’ils suivent un croisement interspe′cifique ou un doublement chromosomique et ils touchent de manie`re pre′fe′rentielle le ge′nome parental le plus grand.Les auteurs discutent des ro?les partage′s que jouent les changements ge′ne′tiques et e′pige′ne′tiques dans l’homoge′ne′isation de la taille des ge′nomes parentaux ainsi que dans l’e′ta-blissement et la stabilisation des espe`ces polyplo?¨des

Mots-cle′s:restructuration des ge′nomes,Tritice′es,hybrides synthe′tiques,polyplo?¨des.

[Traduit par la Re′daction]

Introduction

Polyploidy is a major mode of evolution in plants,which involves two or more genomes being joined into the same nucleus.It has been estimated that30%–70%of plant spe-cies are of polyploid origin,an assessment that is approach-ing100%if paleopolyploids are included(Wendel2000; Wolfe2001).Polyploids are classified into autopolyploids

Received23June2010.Accepted5November2010.Published on the NRC Research Press Web site at genome.nrc.ca on18February 2011.

Corresponding Editor:T.Schwarzacher.

M.Bento,W.Viegas,and M.Silva.1Centro de Bota?nica Aplicada a`Agricultura,Secc?a?o de Gene′tica,Instituto Superior de Agronomia, Technical University of Lisbon,Tapada da Ajuda1349-017Lisboa,Portugal.

https://www.sodocs.net/doc/1511700526.html,DA-ARS,Plant Genetics Research Unit,University of Missouri,Columbia,MO65211-7020,USA.

1Corresponding author(e-mail:manuelasilva@isa.utl.pt).

175

and allopolyploids based on the origin of the component ge-nomes and can be represented by many different ploidy lev-els.An autopolyploid results from the doubling of a diploid genome,and an allopolyploid is formed by the combination of two or more different,but usually related,genomes through hybridization between distinct species or genera.Gene redundancy in polyploids is obvious and leads to new expression patterns,which can generate developmental nov-elty and the appearance of new phenotypes,producing spe-cies with a higher degree of genome plasticity when compared with their progenitors (Chen 2007).Furthermore,the loss of self-incompatibility,gain of asexual reproduction,and higher levels of heterozygosity can be fixed in allopoly-ploids (Comai 2005).These modifications can increase fit-ness,which may explain the widespread occurrence of polyploids in plants.

Newly synthesized polyploids,with precise known pro-genitors,are excellent materials to study the emergence of early and late evolutionary genetic and epigenetic events.This approach has been widely applied in many species,such as wheat (Triticum spp.),Arabidopsis ,Brassica ,cotton (Gossypium spp.),and triticale (?Triticosecale )(Dong et al.2005;Liu et al.2001;Ma et al.2004;Ma and Gustafson 2006;Madlung et al.2005;Ozkan et al.2001;Salmon et al.2005).In synthesized polyploids,genetic and (or)epige-netic changes were observed,although their rate,type,and degree are markedly different between distinct polyploids (Chen 2007;Ma and Gustafson 2008).Allopolyploid ge-nomes experience two different phases:a revolutionary phase,occurring immediately after hybridization that is re-sponsible for rapid genetic and epigenetic changes;and an evolutionary phase that corresponds to long-term events,such as slow changes in DNA sequences and functional al-terations over time (Feldman and Levy 2005;Levy and Feldman 2002).

Triticale,the first synthesized amphidiploid cereal,is a chromosome-doubled intergeneric hybrid that can be obtained by the cross of distinct wheat species (Triticum spp.,AA,AABB,and AABBDD)and rye (Secale cereale L.,RR),pro-ducing various genome combinations and ploidy levels,such as tetraploid AARR,hexaploid AABBRR,and octoploid AABBDDRR.When compared with other allopolyploids,tri-ticale is a very complex genome because of its high ploidy level,large genome size,and the distant relationships between parental genomes.However,because of its short history and accumulated pedigree knowledge,it becomes a very useful model species to study evolutive processes mediated by poly-ploidization.Synthetic allotetrapolyploids involving Aegilops spp.and Triticum spp.have also been analyzed in comparison with their parental species in an attempt to simulate natural wheat allopolyploids.The aims of this review are to summa-rize findings obtained so far in Triticeae polyploid species and compare results with other allopolypoid species.

Polyploid genomic analysis

Overall,genomic sequence changes have been extensively studied in Triticeae polyploids involving different octoploid and hexaploid triticales,the corresponding F 1hybrids,and their respective parental genomes to assess polyploidization-induced genome readjustments using molecular marker tech-T a b l e 1.S u m m a r y o f t h e g e n o m i c a l t e r a t i o n s d e t e c t e d i n t r i t i c a l e u s i n g d i s t i n c t m e t h o d o l o g i e s o f g e n o m i c a n a l y s i s .

A F L P a

R F L P b

I R A P –R E M A P –I S S R c N o c h a n g e L o s s N o v e l d

N o c h a n g e L o s s N o v e l d

N o c h a n g e L o s s N o v e l d

W h e a t s p e c i f i c

93322799—188353—–516—(76.9)(23.1)—(97.3)(2.7)—(89.5)(10.5)—R y e s p e c i f i c

25004808—395633—2630—(34.2)(65.8)—(38.4)(61.6)—(46.4)(53.6)—S h a r e d

2283495—1975—580—(82.2)(17.8)—(97.5)(2.5)—(100)(0)—N o v e l

——1535——250——6——(9.8)——(9.2)——(4.2)T o t a l

141158102—2475691—13536—(63.5)

(36.5)—(78.2)(21.8)—(78.9)(21.1)—

N o t e :P e r c e n t a g e s a r e d i s p l a y e d i n (p a r e n t h e s e s ).

a

A F L P r e s u l t s a r e a c o m p i l a t i o n o f t h e r e s u l t s p u b l i s h e d b y M a e t a l .(2004)a n d M a a n d G u s t a f s o n (2006).b

R F L P r e s u l t s a r e p r e s e n t e d i n M a e t a l .(2004).c I R A P –R E M A P –I S S R r e s u l t s a r e p r e s e n t e d i n B e n t o e t a l .(2008).d P e r c e n t a g e s a r e c a l c u l a t e d i n r e l a t i o n t o t h e n u m b e r o f t r i t i c a l e o b s e r v e d b a n d s .%n o v e l =n o v e l /(n o c h a n g e +n o v e l )?100.

176Genome Vol.54,2011

niques,such as amplified fragment length polymorphism (AFLP)and restriction fragment length polymorphism (RFLP)analysis(Ma et al.2004;Ma and Gustafson2006). AFLP analysis was used to study different synthetic wheat allotetraploids between Aegilops spp.and Triticum spp.,F1 hybrids,and their homozygous diploid parents(Dong et al. 2005;Shaked et al.2001).Large-scale AFLP studies were implemented to obtain an unbiased genome-wide estimation of the occurrence of genomic sequence variation using dif-ferent restriction enzymes,namely Eco RI–Mse I primers, which amplify repetitive sequences(Dong et al.2005;Ma et al.2004;Ma and Gustafson2006;Shaked et al.2001) and Pst I–Mse I primers,which predominantly target low-copy sequences most present in distal gene-rich regions,as Pst I is highly sensitive to the cytosine status(Milla and Gustafson2001;Young et al.1999).Furthermore,coding sequence variation induced by polyploidization in Triticeae was investigated using cDNA-probed RFLP analyses(Ma et al.2004).

Utilizing a wide series of primer combinations,octoploid triticale amphidiploids and their wheat and rye parental ge-nomes were analyzed using inter-retrotransposon amplified polymorphism(IRAP),retrotransposon-microsatellite ampli-fied polymorphism(REMAP),and inter-simple sequence re-peat(ISSR)techniques(Bento et al.2008).IRAP,REMAP, and ISSR are PCR-based molecular marker techniques ini-tially designed to identify different barley(Hordeum vulgare L.)cultivars(Kalendar et al.1999)combining primers de-signed for long terminal repeat(LTR)retrotransposons, which have a very important role in genome evolution and speciation owing to their dynamics and potential mobility (Vitte and Panaud2005),and(or)microsatellites,which constitute polymorphic loci present throughout nuclear DNA,preferentially associated with retrotransposons in ce-reals(Ramsay et al.1999).Primers designed to evaluate LTRs point outwards and amplify retrotransposon-flanking sequences,thus allowing for the detection of retrotransposon insertional polymorphisms(Kalendar and Schulman2006). Recently,a more specific molecular marker system in-volving single sequence repeat(SSR),originally designed to study unique sequences containing microsatellites in the wheat genome(Ro¨der et al.1998),was used to study varia-tion induced by polyploidization in triticale with different combinations of wheat and rye parents(Tang et al.2008). The above molecular marker systems were crucial to dis-closing genomic modifications induced by polyploidization, allowing the detection of extensive changes accessed by al-terations in banding profiles.AFLP and RFLP analyses al-lowed for a genome-wide range evaluation offering the possibility to differentiate between genome euchromatic and heterochromatic fractions.Whereas,IRAP,REMAP,and ISSR,which are unaffected by DNA methylation(Kalendar and Schulman2006)and specific for repetitive motifs such as retrotransposons(Vitte and Panaud2005),allowed for the detection of rearrangements involving both repetitive and coding sequences(Bento et al.2008).

Genome rearrangement events revealed by band losses

The results obtained by the analysis of triticale polyploids were re-evaluated and have been summarized in Table1, and clearly disclosed the high level of genome restructuring events associated with polyploid establishment(Bento et al.

Table2.Re-evaluation of collected data of percent parental band loss/elimination by sequence type in octoploid and hexaploid triticales.

%elimination

Octoploid Hexaploid

Analysis Sequence type Parental genome CS?I H?K C?S C?U AFLP a Repetitive W24.825.244.047.4

R61.165.562.567.8 Low copy W8.7 6.614.815.6

R69.869.761.168.8 RFLP b Coding W 2.2 1.2 5.5 2.4

R64.860.862.257.9 IRAP–REMAP–ISSR c Repetitive motifs-flanking regions W10.5———

R53.6———Note:W,wheat;R,rye(2n=2x);CS,‘Chinese Spring’(2n=6x);I,‘Imperial’;H,‘Holdfast’(2n=6x);K,‘King II’;C,‘Cocorit71’(2n=4x);

S,‘Snoopy’;U,‘UC90’.Percentages were calculated separately for each parent and shared bands are not taken into consideration(results for eliminated shared bands are not shown).%elimination=(specific type of parental bands eliminated)/(total of specific type of parental bands detected)?100.

a AFLP results are a compilation of the results published by Ma et al.(2004)and Ma and Gustafson(2006).

b RFLP results are presented in Ma et al.(2004).

c IRAP–REMAP–ISSR results are presente

d in Bento et al.(2008).

Table3.Collected data from Dong et al.(2005)and

Shaked et al.(2001)on percent parental band loss/

elimination using AFLP(repectitive sequence type)in

Aegilops?Aegilops,Aegilops?Triticum,and

Triticum?Aegilops polyploid genotypes.

Polyploid genotype Parental

genome

%elimination

of total bands

As?Au As14

Au0.5

Al?Tu Al12.2

Tu11.4

Tt?At Tt21

At12.3

Note:As,Ae.sharonensis(2n=2x);Au,Ae.umbellulata

(2n=2x);Al,Ae.longissima(2n=2x);Tu,T.urartu(2n=

2x);Tt,T.turgidum(2n=4x);At,Ae.tauschii(2n=2x).

Bento et al.177

2008;Kashkush et al.2002;Ma et al.2004;Ma and Gustaf-son 2006;Tang et al.2008).Although there are several studies regarding the evaluation of genomic restructuring events in Triticeae hybrids,besides the studies of Dong et al.(2005)and Shaked et al.(2001)(reviewed in Table 2),none discriminate for levels of parental-specific alterations (Feldman et al.1997;Kashkush et al.2002;Ozkan et al.2001;Ozkan et al.2003;Tang et al.2008).The data analy-sis is based on the comparison between parental lines and polyploid gel profiles.Thus,all the bands present in parental gel profiles are considered parental bands and shared bands are the ones present in both parental lines.Conserved bands are bands present in parental profiles and maintained in the polyploid profile,whereas absent bands are bands present in the parental profiles that are missing in the polyploid,indi-cating the occurrence of a rearrangement event in the poly-ploid.On the other hand,novel bands are the ones that are present in the newly formed polyploid and absent in parental gel profiles,indicating the occurrence of genome rearrange-ments.The overall examination of the published results re-veal that the variation detected in triticale is significantly higher than that observed in other synthetic polyploids,namely wheat species complexes and Brassica (Song et al.1995).Such marked differences in polyploid behavior could be due to triticale being of intergeneric origin that may have lead to additional enhanced modifications to parental ge-nomes,thus stabilizing the newly formed polyploid.This hypothesis is reinforced by studies in natural and newly syn-thesized wheat interspecific polyploids,which suggest lower levels of parental genome restructuring in comparison with triticale (Dong et al.2005;Feldman et al.1997;Liu et al.1998;Ozkan et al.2001).Similarly,genetic distance is very important when analyzing hybrids within the same genus;for example,crosses between Brassica rapa and Brassica nigra revealed a higher genome variation than the crosses between the more closely related species B.rapa and Bras-sica oleracea (Song et al.1995).The same was observed in hybrids among members of the Triticeae where an interspe-cific cross between Aegilops sharonensis and Aegilops um-bellulata revealed lower variation (6.7%)than an intergeneric cross between Aegilops longissima and Triticum urartu (11.8%)(Shaked et al.2001)or Triticum turgidum and Aegilops tauschii (17.2%)(Dong et al.2005).

The rearrangements detected in triticale by AFLP–RFLP and IRAP–REMAP–ISSR analysis (Bento et al.2008;Ma et al.2004;Ma and Gustafson 2006;Tang et al.2008)es-tablished the disappearance of bands from both parental ori-gins and the emergence of novel bands absent in the progenitor’s banding profiles.The appearance of novel bands was also described in Brassica polyploids (Song et al.1995).Not surprisingly,the triticale genome analyses clearly demonstrated that the disappearance of parental bands was much more frequent than the appearance of novel bands.The percentage of band disappearance (Table 1)var-ied between 36.5%(detected by AFLP)and 21.1%(detected by IRAP–REMAP–ISSR),whereas the appearance of novel bands was 9.8%(detected by AFLP),9.2%(detected by RFLP),and 4.2%(detected by IRAP–REMAP–ISSR)(Bento et al.2008;Ma et al.2004;Ma and Gustafson 2006).Simi-lar results were reported in other polyploids involving Triti-cum ,Brassica ,and Spartina (Dong et al.2005;Kashkush et

T a b l e 4.N u m b e r a n d p e r c e n t a g e (i n p a r e n t h e s e s )o f b a n d s l o s t b e f o r e a n d a f t e r c h r o m o s o m e d o u b l i n g d e t e c t e d b y (M a a n d G u s t a f s o n 2006)i n w h e a t –r y e h y b r i d s .

O c t o p l o i d

H e x a p l o i d

C S ?I

H ?K

C ?S C ?U S e q u e n c e t y p e P a r e n t a l g e n o m e F 1

T T o t a l a

F 1

T T o t a l a

F 1

T T o t a l a

F 1

T T o t a l a

R e p e t i t i v e

W

104156109450655359615662715593602(9.5)(14.3)(23.8)(9.3)(12.1)(21.5)(15.3)(24.9)(40.2)(25.7)(15.4)(41.2)R

16169403124292321364629810235228(40.0)(17.1)(57.1)(53.4)(12.5)(65.9)(45.6)(15.4)(61.1)(44.7)(15.4)(60.1)L o w c o p y

W

184593981261626405262030427(1.9)(4.8)(6.7)(1.3)(1.9)(3.2)(4.9)(7.6)(12.5)(4.7)(7.0)(11.7)R

284138646165453141448137911663285(44.0)

(21.4)(65.3)(52.5)(14.3)(66.9)(38.0)(21.4)(59.4)(40.7)(22.1)(62.8)

N o t e :W ,w h e a t ;R ,r y e ;F 1,b a n d s e l i m i n a t e d i n F 1h y b r i d s ;T ,b a n d s e l i m i n a t e d i n t r i t i c a l e s a f t e r c h r o m o s o m e d o u b l i n g (r e s u l t s f o r s h a r e d b a n d s a r e n o t p r e s e n t e d );C S ,‘C h i n e s e S p r i n g ’;I ,‘I m p e r i a l ’;H ,‘H o l d f a s t ’;K ,‘K i n g I I ’;C ,‘C o c o r i t 71’;S ,‘S n o o p y ’;U ,‘U C 90’.

a

%o f t o t a l b a n d s l o s t i n h y b r i d p l u s l o s t i n t r i t i c a l e .

178

Genome Vol.54,2011

al.2002;Salmon et al.2005;Shaked et al.2001;Song et al.1995).Sequence restructuring,therefore,seems to be a widespread phenomenon associated with newly formed pol-yploids (Leitch and Bennett 2004).The exception to genome downsizing was reported in cotton (Gossypium )polyploids (Liu et al.2001)where genomic changes were not detected by AFLP,although a reduction in C-DNA values was ob-served when these polyploids where compared with parental genomes (Bennett 1977;Bin and Kadir 1976).

Genome rearrangement frequencies in triticale depend on sequence types and wheat ploidy levels

Sequence rearrangements are not restricted to repetitive and noncoding sequences,as coding sequences,regulatory elements,and promoter regions appear to also be affected by polyploidization (Bento et al.2008;Ma et al.2004;Tang et al.2008),although in different levels.In triticale,repetitive sequences were found to be more frequently rear-ranged than low-copy and coding sequences (Ma et al.2004).Published data indicated that 42%,31%,and 22%of bands were lost from repetitive,low-copy,and coding se-quences,respectively (values presented in Ma and Gustafson 2008).Wheat-specific sequence rearrangements are also highly affected by the kind of sequence being analyzed.In octoploid and hexaploid triticale,the level of wheat-specific band loss varied,being approximately 25%and 46%,7%and 15%,and 1.5%and 4%for repetitive,low-copy,and coding sequences,respectively (Table 2).In contrast with the marked differences of wheat-specific band losses,rye-specific bands appear to be lost at similar percentages inde-pendent of the type of sequence,ranging between 57.9%and 69.8%(Table 2).

The data published by Ma et al.(2004)and Ma and Gus-tafson (2006)showed that the level of band loss in triticale was distinct for each parental genome (Table 2).Triticale genotype analyses demonstrate that the level of rye parental genome band elimination is higher than the observed level for wheat genome.The maximum percent of wheat-specific band elimination was 47.4%(detected by AFLP in hexa-ploid triticale),whereas rye-specific band elimination ranged between 53.6%(detected in octoploid triticale by IRAP–

REMAP–ISSR analyses)and 69.8%(detected in octoploid triticale by AFLP analysis).Differences between percen-tages of rye and wheat-specific band elimination in hexa-ploid triticales were 18.5%by AFLP analysis and 62.6%in octoploid triticale by RFLP analysis.

Gill (1991)suggested that the rye paternal genome being exposed to the adverse environment of maternal wheat cyto-plasm in newly formed hybrids could explain its preferential restructuring in triticale.Ma and Gustafson (2008)also sug-gested that the instability of rye–wheat hybrids may be due to nuclear–cytoplasmatic interactions.However,the Triti-ceae studies of Dong et al.(2005)and Shaked et al.(2001)contradict the paternal preferential elimination hypothesis,as maternal genome elimination was observed in synthetic wheat (Table 3).When Aegilops speltoides was crossed as female and as male in a study designed to ascertain the ef-fects of cytoplasm on the pattern and rate of sequence elim-ination,no cytoplasm effects were detected (Ozkan et al.2001).

On the other hand,as triticale results from an intergeneric hybridization between a polyploid (wheat)and a diploid spe-cies (rye),we can consider that wheat has already been sub-ject to genetic and (or)epigenetic modifications during its evolution,thus being more adapted to the polyploidy condi-tion than rye genome.A detailed analysis of data presented in Table 2reveals a plausible correlation between genome rearrangement percentages and wheat ploidy levels.How-ever,such correlations were absent in the cross between T.turgidum and Ae.tauschii (using enzymes not sensible to methylation),as more genome modifications were de-tected in the maternal tetraploid genome than in the pater-nal diploid genome (Table 3).

A higher global genome variation was observed in hexa-ploid (40%)than in octoploid triticale (~30%)(Ma and Gus-tafson 2008),reinforcing previous data (Boyko et al.1984)showing that DNA content reduction was also higher in hex-aploid than in octoploid triticale (28%–30%and 9%,respec-tively).Although the elimination level of rye-specific bands appears similar both in hexaploid and octoploid triticale,the elimination rate of wheat-specific bands is much higher in hexaploid triticale (for details see Table 2).The mean elimi-nation rate of wheat-specific repetitive sequences in hexa-ploid triticale was 45%and 25%in octoploid triticale,

Table 5.Number and percentage (in parentheses)of bands lost before and after chromosome doubling detected by (Shaked et al.2001)in Aegilops ?Aegilops and Aegilops ?Triticum hybrid genotypes.

As ?Au

Al ?Tu Sequence type Parental genome F 1A Total a F 1A Total a Global Repetitive b

As 204171———(11.7)(2.3)(14)———25Au 01202———(6.7)

(0)(0.5)(0.5)———Al ———1210180———(15.0)(27.5)(12.2)41Tu

———118166(11.8)

(0.6)

(10.8)

(11.4)

Note:As,Ae.sharonensis ;Au,Ae.umbellulata ;Al,Ae.longissima ;Tu,T.urartu ;F 1,bands eliminated in F1hybrids;A,bands eliminated in allotetraploids after chromosome doubling.

a %of total bands lost in hybrid plus lost in allotetraploid.b

Results are only for non-methylation-sensitivite enzymes.

Bento et al.

179

revealing a higher buffering capacity of hexaploid wheat ge-nome to avoid large numbers of sequence rearrangements in triticale.Such correlations between parental ploidy level and genome alteration rate have not been established in other species such as cotton and wheat (Aegilops ?Triticum )pol-yploids (Liu et al.1998;Ozkan et al.2001).

The results indicate that each triticale parental genome is subjected to distinct regulatory systems.In the wheat-origin genome,each type of sequence seems to have different rele-vancies in genome adaptation through polyploidization,and the elimination of different sequences is apparently con-trolled accordingly.Contrastingly,the rye-origin genome ap-pears to be highly restructured upon polyploidization independently of sequence type considered.

Parental genomes are differently

restructured during hybridization and polyploidization

The data obtained for two hexaploid and two octoploid triticales,their respective parental lines,and their corre-spondent F 1hybrids (Ma and Gustafson 2006)clearly dem-onstrated the occurrence of two major stages of restructuring events.First during the formation of the wide hybrid,fol-lowed by a second after chromosome doubling of the hy-brid.The reanalyzed results are summarized in Table 4,revealing during the first stage an immediate and drastic re-sponse to hybridization,whereas in the second stage a con-tinuous process of changes occurring at a slower rate (Ma and Gustafson 2006).Similar results,presented in Table 5,were described by Shaked et al.(2001)in Aegilops ?Aegilops and Aegilops ?Triticum crosses and also reported in Aegi-lops ?Triticum and Spartina F 1hybrids,although not so pronounced (Ozkan et al.2001;Salmon et al.2005).

The enhanced modification levels observed when rye ge-nome interacts either with hexaploid or tetraploid wheat ge-nomes appears to be mainly the result of adjustments occurring immediately after hybridization.Curiously,the rate of band elimination observed after F 1hybrid chromo-some doubling is very similar for wheat and rye repetitive sequences,ranging between 12%and 17%,for most triti-cales except one hybrid analyzed by Ma and Gustafson (2006)in which the level of wheat repetitive bands lost was almost 25%.Moreover,Ma and Gustafson (2006)noted in two sets of wheat–rye hybrids that hexaploid wheat repeti-tive sequences had a higher buffer capacity and less changes in comparison with tetraploid wheat genome (24.8%and 25.2%versus 44%and 47.4%,respectively).

In all wheat–rye F 1hybrids and correspondent triticale studied (Ma and Gustafson 2006),a preferential elimination of bands associated to repetitive rather than low-copy se-T a b l e 6.P a r e n t a l g e n o m e p r e f e r e n t i a l r e s t r u c t u r i n g i n T r i t i c e a e p o l y p l o i d s y s t e m s .

M a t e r n a l g e n o m e

P a t e r n a l g e n o m e

P l o i d y 1C (M b p )%e l i m i n a t i o n P l o i d y 1C (M b p )%e l i m i n a t i o n H i g h e r e l i m i n a t i o n l e v e l S o u r c e A e g i l o p s s h a r o n e n s i s ?A e g i l o p s u m b e l l u l a t a 2n =2x =14

6909

14.0

2n =2x =14

4949

0.5

M a t e r n a l

S h a k e d e t a l .2001

A e g i l o p s l o n g i s s i m a ?T r i t i c u m u r a r t u 2n =2x =14

5929

12.2

2n =2x =14

4827

11.4

M a t e r n a l

S h a k e d e t a l .2001

T r i t i c u m t u r g i d u m ?S e c a l e c e r e a l e 2n =4x =28

12030

27.6

2n =2x =14

8110

64.0

P a t e r n a l

M a e t a l .(2004):M a a n d G u s t a f s o n 2006T r i t i c u m a e s t i v u m ?S e c a l e c e r e a l e

2n =6x =42

1697914.22n =2x =148110

66.2

P a t e r n a l

M a e t a l .(2004):M a a n d G u s t a f s o n 2006;B e n t o e t a l .2008T r i t i c u m t u r g i d u m ?A e g i l o p s t a u s c h i i

2n =4x =281203021.02n =2x =14

5027

12.3M a t e r n a l

D o n g e t a l .2005

Table 7.DNA 1C-value and cell cycle time (CCT)in triticale and wheat and rye parental species.Species

1C-value a (pg)CCT b (h)Secale cereale ‘UC90’

8.312.0Triticum turgidum ‘Cocorit’

12.2812.0?Triticosecale ‘Cocorit’?‘UC90’

16.812.0

a Plant DNA C-values database,Royal Botanic Gardens,Kew,UK.b

Kidd et al.1987.

180

Genome Vol.54,2011

quences was observed concerning the wheat parental ge-nome.Conversely,rye-origin repetitive and low-copy se-quences were altered in similar level in the hybrid and after chromosome doubling.Therefore,it is clear that bands asso-ciated with coding sequences are comparatively more elimi-nated in rye than in wheat.Such preferential genome elimination can drastically reduce homeologues gene copies avoiding gene redundancy,favoring a‘‘diploid’’behavior and further polyploid stabilization,as proposed(Feldman et al.1997).

Size matters in triticale genome rearrangements:larger genomes are more affected

As described earlier,major genomic restructuring events were identified in triticale at higher percentages than in any other polyploid studied,which affected variation in repeti-tive,low-copy,and coding sequences present in the genome. Analysis of triticale confirmed early suggestions on the mechanisms involved in polyploidization adjustment,but also revealed new concerns.The idea that sequence elimina-tion is a major event involved in the stabilization of newly formed polyploids was reinforced by the results reviewed, as the overall number of sequences lost confirmed previous descriptions on genome size decrease in triticale(Boyko et al.1984).In the studies of Ozkan et al.(2003)and Eilam et al.(2008)an extensive list of genome downsizing examples in Aegilops?Triticum hybrid genotypes was presented. Moreover,it was recently shown that the absence of rye-origin bands in wheat–rye hybrid genotypes resulted from sequence elimination rather than from changes to primer annealing sites(Bento et al.2010).

The higher degree of paternal genome elimination ob-served in triticale is not the general rule that has been ob-served in other newly formed polyploids.In Table6, preferential parental genome elimination is presented for some Triticeae polyploids,showing that the maternal ge-nome can also show preferential sequence elimination,con-tradicting the hypothesis of Gill(1991).The results compiled clearly demonstrated that the genome suffering more modifications during polyploidization was always the larger one(comparing DNA contents per haploid genome), independently of their maternal or the paternal status.Thus, the results collected in this review clearly point out,for the first time,the tendency in cereal-wide hybridization for pa-rental genome size homogenization,which preferentially af-fects the larger genome to stabilize the newly formed polyploid https://www.sodocs.net/doc/1511700526.html,rge scale rearrangement events are also observed resulting from the loss of telomeric heterochroma-tin,a mechanism used to obtain a more balanced nucleotype in triticale(Jouve et al.1989).Bernardo et al.(1988)dem-onstrated a clear negative effect of rye heterochromatin on triticale meiotic pairing and that the loss of telomeric heter-ochromatic blocks are related to yield increase in hexaploid triticale(Gustafson and Bennett1982).This phenomenon can be the outcome of the relation between nuclear DNA content and the speed of DNA replication(Francis et al. 2008).In fact,the larger parental genome in a hybrid nu-cleus may not be able to complete the cell cycle by the time of telophase and(or)cell wall formation,thus inducing DNA elimination through breakage–fusion bridges as previ-ously observed in the early endosperm development of wheat–rye hybrids(Bennett and Gustafson1982;Gustafson and Bennett1982).Moreover,those sequence elimination events will certainly preferentially affect late replication re-petitive fractions of the genome,namely the dense rye heter-ochromatic subtelomeric domains(Bennett1977;Neves et al.1997).

That hypothesis is reinforced by the effect of DNA C-values in cell cycle duration on correlations between DNA amount,nuclear volume,and cell cycle length in angio-sperms(Van’t Hof and Sparrow1963)and in triticale (Kaltsikes1971;Bennett and Kaltsikes1973).Recently, the analysis of cell cycle duration in110monocots and eu-dicots species were plotted against the respective nuclear DNA C-values(Francis et al.2008),and a highly signifi-cant regression was observed for all species analyzed,inde-pendently of their ploidy level.However,Kidd et al. (1987)presented values for hexaploid triticale in compari-son with parental species(Table7)and surprisingly dem-onstrated that,although polyploidization leads to an increase on genome size,cell cycle time(CCT)values are constant for progenitors and the polyploid species.They also showed the maintenance of stable cell cycle lengths in hexaploid wheat where the parental CCT values are 11.4h in Ae.tauschii,and ranged from11.0h to13.9h in T.turgidum,but doesn’t exceed14.0h in the allopoly-ploid T.aestivum.The clear correlation between nuclear DNA amounts and cell cycle length appears to be associ-ated with genome heterochromatic fraction dimension(re-viewed in Redi et al.2001)and with the speed of DNA replication(Francis et al.2008).This is where genome re-structuring meets epigenetic remodeling of parental ge-nomes allocated to the same nuclear background.In fact, more than just genome rearrangements are necessary for the adjustment of both parental genomes following poly-ploidization,chromatin remodeling also mediates required changes when two species share a common hybrid nucleus. Viegas et al.(2002)proposed a model explaining chroma-tin-imprinting control of nucleolar dominance in polyploid species,based on the importance of genome size in such interactions.With the Viegas et al.(2002)model,differen-ces in genome size owing to repetitive DNA sequence var-iation allocated in heterochromatin domains should induce the need for greater elimination events in the larger rye ge-nome,to properly‘‘accommodate’’in the hybrid nucleus. Following such hypothesis,more intimate associations be-tween heterochromatic domains should also occur,modify-ing expression patterns of neighboring genes.Epigenetic functional fine tuning of parental genomes together with preferential rearrangements of the larger parental genome will,therefore,certainly assist polyploid genome downsiz-ing.Genetic and epigenetic modifications seem,therefore, crucial to establish the diploid-like behavior and speciation of polyploid genomes,as proposed by Ma and Gustafson (2005).

Acknowledgements

Miguel Bento is funded by a doctoral scholarship(SFRH/ BD/28657/2006)by Fundac?a?o para a Cie?ncia e a Tecnolo-gia,Portugal.This research was financed by Fundac?a?o para

Bento et al.181

a Cie?ncia e a Tecnologia(Project PTDC/BIA-BEC/101964/ 2008).

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