Deciphering the evolutionary interplay between subgenomes following polyploidy: A paleogenomics approach in grasses

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R E S E A R C H A R T I C L E

UNVEILING GRASS EVOLUTIONARY HISTORY FROM

ANCESTRAL GRASS KARYOTYPES

Th

e fl owering plants (angiosperms) contain the major clades of

eu-dicots (~275,000 species) and monocots (~65,000 species) and the

smaller groups of magnoliids (~2500 species), Chloranthaceae (~50

species), and Ceratophyllum (5 species) ( Soltis et al., 2008 , 2011 ).

Th

e monocots and eudicots, the two largest and most diverse groups,

accounting respectively for 20% and 75% of modern angiosperm

species, are clades of choice to investigate the forces promoting

species evolution through polyploidization (genome doubling) or

whole-genome duplication (WGD) ( Van de Peer et al., 2009a , b ).

Reconstructing ancestral genomes from the comparison of

modern karyotypes, i.e., the fi eld of paleogenomics research, is

based on the identifi cation of duplications (or any shuffl

ing events)

at orthologous positions between modern species, defi ning

proto-chromosomes (i.e., independent groups of syntenies and paralogies

also referenced as contiguous ancestral regions [CARs]). Th

e

de-duced evolutionary history is then based on the smallest number

of shuffling operations (ancestral chromosome fusion, fission,

inversion, and translocation events) able to account for the

transi-tion from the inferred ancestral karyotypes to the modern genomes

( Salse et al., 2009; Salse, 2012 , 2016 ).

In grasses, for monocots, we inferred an ancestral grass

karyo-type (AGK) structured in seven protochromosomes containing

16,464 protogenes (taking into account gene conservation between

species), with 8581 ordered (taking into account gene adjacency

conservation between species) and with a minimal gene space

physical size of 33 Mb ( Murat et al., 2010 , 2014a , 2014b ). Th

is

an-cestor went through a paleotetraploidization event (consisting of

seven duplicated blocks shared in the modern monocots) dating

back to more than 90 million years ago (Ma) ( Salse et al., 2008 ,

2009 ; Murat et al., 2010 ; Wang et al., 2015 ) and followed by two

symmetric reciprocal translocations, one centromeric (centromeric

chromosome fusion [CCF]) and one telomeric (telomeric

chromo-some fusion [TCF]) and two asymmetric reciprocal translocations

to reach a 12-chromosome intermediate ( Murat et al., 2014a ,

2014b ). A centromeric chromosome fusion (CCF) consists of a

process during which an entire chromosome is inserted (i.e., one

fusion called Cfus in Fig. 1 ) by its telomeres into a break (i.e., one

fi ssion called Cfi s in Fig. 1 ) in the centromeric region of another

chromosome (CCF = 1 fusion + 1 fi ssion and also termed a nested

chromosome fusion NCF; IBI, 2010 ). A telomeric chromosome

fu-sion (TCF) consists of an end-to-end joining of two chromosomes

at their telomeres (CCF = 1 fusion, without fi ssion and also termed

tip-to-tip joining). From the fusion of two ancestral chromosomes,

1_{Manuscript received 2 November 2015; revision accepted 1 March 2016.}

INRA/UBP UMR 1095 Génétique, Diversité et Ecophysiologie des Céréales, Laboratory of Paleogenomics & Evolution, 5 chemin de Beaulieu 63100 Clermont Ferrand, France

2_{E-mail: jsalse@clermont.inra.fr; phone: +33(0)473624380; fax: +33(0)473624453} doi:10.3732/ajb.1500459

I N V I T E D PA P E R

For the Special Issue: The Evolutionary Importance of Polyploidy

Deciphering the evolutionary interplay between

subgenomes following polyploidy: A paleogenomics

approach in grasses

1

Jérôme Salse 2

How did plant species emerge from their most recent common ancestors (MRCAs) 250 million years ago? Modern plant genomes help to address such key questions in unveiling precise species genealogies. The fi eld of paleogenomics is undergoing a paradigm shift for investigating species evolution from the study of ancestral genomes from extinct species to deciphering the evolutionary forces (in terms of duplication, fusion, fi ssion, deletion, and translocation) that drove present-day plant diversity (in terms of chromosome/gene number and genome size). In this review, inferred ancestral karyotype genomes are shown to be powerful tools to (1) unravel the past history of extant species by recovering the variations of ancestral genomic compartments and (2) ac-celerate translational research by facilitating the transfer of genomic information from model systems to species of agronomic interest.

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while CCF delivers a monocentric chromosome, TCF delivers a

di-centric chromosome where one centromere is lost to return to

monocentry through pericentric inversion ( Schubert and Lysak,

2011 ).

All investigated grass genomes can then be reconstructed from

this postpolyploidy ancestral karyotype of 12 protochromosomes

( Fig. 1 ) following CCF, TCF, translocation, or inversion events

( Fig. 1 ). Rice has retained the n = 12 AGK structure and has been

proposed as the slowest-evolving species among the grasses ( Wang

et al., 2015 ), whereas the other species experienced numerous

chro-mosome rearrangements to reach the present-day karyotypes

( Murat et al., 2010 , 2014a , b ). Furthermore, it is possible to represent

the chromosome number for any modern grass species by a

karyo-typic equation refl ecting the evolutionary events, such as duplications

(

× 2), fusions (−Y), fi ssions (+Z), that took place during evolution.

For example in Table 1 , the maize karyotypic equation is [12 − 4 + 2]

× 2 + 7 − 17, refl ecting that the monocot ancestral intermediate

with 12 chromosomes went through 4 fusions (i.e., two CCF) and 2

fi ssions to reach a 10-chromosome Panicoideae intermediate,

fol-lowed by one WGD (to form a 20-chromosome intermediate) and

fi nally 7 CCFs and 10 TCFs (consisting of at least 7 fi ssions and

17 fusions) to reach the modern genome structure of 10

chromo-somes. Such ancestral chromosome fusion events (either TCF or

CCF, Fig. 1 ) that reduce the number of chromosomes in the

mod-ern karyotypes from their postpaleopolyploid ancestors are called

asymmetric and symmetric reciprocal translocations in

chromo-somal mutagenesis approaches and cytogenetic studies ( Schubert

and Lysak, 2011 ). A SyntenyViewer tool ( Fig. 2 ) is available to the

scientifi c community to have access to the inferred AGK to navigate

between grass species. Th

e SyntenyViewer tool delivers a precise

paleogenomics-based repertoire of paralogs/orthologs to perform a

translational research approach in improving (1) complex genome

FIGURE 1 Grass genome evolution from ancestral grass karyotypes (AGKs) (adapted from Murat et al., 2010 , 2014a , b ). Present-day grass genomes (bottom) are represented with color codes to illustrate either (top) the evolution of segments from their founder AGK progenitor with seven proto-chromosomes (referenced as Ax, synteny painting) or (bottom) the mosaic of dominant and sensitive blocks inherited from polyploidization (refer-enced as D in red or S in blue, dominance painting). Whole-genome duplication events that have shaped the structure of the modern grass genomes during their evolution from AGK are indicated as red dots. The geological periods are indicated on the tree branches as millions of years ago (Ma). Evolutionary genome shuffl ing events such as chromosomal fusions, fi ssions, and translocations are abbreviated on the tree branches: CCF, centromeric chromosome fusion; Cfi s, chromosome fi ssion; Cfus, chromosome fusion; INV, inversion; TCF, telomeric chromosome fusion; Transl, translocation.

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J U LY 2016 , V O LU M E 103 • S A L S E — PA L E O G E N O M I C S A N D E V O LU T I O N I N G R A S S E S • 1169 T ABLE 1 .

Plant genome data sets used in paleogenomics studies

. Species C ommon name Ref er enc e C hr omosomes G enome f ea tur es a Annota ted genes E v olutionar y f ea tur es b Siz e (Mbp ) / TE (%) K ar y ot ypic equa tion fr om n = 12 A GK c Rounds (R) of WGD O ryza sativ a R ice IR GSP , 2005 12 372 / 39 40,577 12 = 21 + 0 − 0 [0C CF / 0T CF] 1R Br achypodium distachy on Brach ypodium IBI, 2010 5 271 / 28 25,532 5 = 12 + 7 − 14 [7C CF / 0T CF / 11INV ] 1R Hor deum vulgar e Bar ley M ay er et al ., 2011 7 ~5000 / >80 15,719 7 = 12 + 5 − 10 [5C CF/0T CF] 1R Sec ale c er eale R ye M ar tis et al ., 2013 7 7917 / >80 2940 d 7 = 12+ 5 − 10 [5C CF / 0T CF / 6T ransl .] 1R Triticum aestivum Wheat IWGSC, 2014 21 ~17,000 / >80 99,386 21 = (12+ 5 − 10) × 3 [2WGD / 5C CF / 0T CF / 2T ransl .] 3R Lolium per enne R yeg rass Pf eif er et al ., 2013 7 2600 / >80 762 d 7 = 12 + 5 − 10 [5C CF / 0T CF] 1R Sor ghum bic olor Sor ghum Pat erson et al ., 2009 10 659 / 62 34,496 12+ 2 − 4 [2C CF / 0T CF / 5INV ] 1R Setaria italic a M illet Zhang et al ., 2012 9 490 / 46 38,801 12 + 2 − 5 [2C CF / 1T CF / 6INV ] 1R Z ea mays M aiz e Schnable et al ., 2009 10 2365 / 84 32,540 [12 + 2 − 4] × 2 + 7 − 17 [1WGD / 9C CF / 10T CF / 39INV ] 2R a Genome f eatur es ar e r epor ted accor ding t o the inf or mation a

vailable in the initial genome paper (cf

. Ref er ence column). b Ev olutionar y f eatur es ar e r epor ted accor ding t o r

ecent paleogenomics studies (

Murat et al ., 2014a , b ). c The k ar yot ypic equation in volv es whole -genome duplication ( W GD) ( × 2), fi

ssions (+X) and fusions (−Y

), consisting in centr omer ic chr omosome fusions (C CF), t elomer ic chr omosome fusions ( TCF), in versions (INV ), and translocations (T ransl .) r ef er enced within “[ ]” . d M

apped genes or mar

kers

.

assembly, (2) structural and functional gene annotation, or (3)

can-didate gene or marker selection for traits dissection ( Salse, 2013,

2016 ).

UNVEILING GRASS GENOME PLASTICITY FROM ANCESTRAL

GRASS KARYOTYPES

Th

e number of annotated genes observed in the modern

angio-sperm genomes is lower than what can be predicted based on the

reconstructed ancestral gene pool and the number of

polyploidiza-tion events identifi ed, in theory, doubling the number of genes in

the post-WGD karyotypes. As a case example for the grasses that

underwent one (rye, barley, ryegrass, Brachypodium , rice, sorghum,

and setaria), two (maize) or even three (wheat) polyploidization

events, the maize genome should contain 16,464

× 4 = 65,856

mod-ern genes, instead of the current 32,540 annotated genes ( Fig. 1 ),

indicative that the rate of duplicates deletion is just important as

the rate that new genes are born from duplications through WGDs;

these opposite forces have shaped the gene content of modern plant

genomes.

Th

is phenomenon is explained by the observation that

poly-ploidization events are followed by a dipoly-ploidization (or

fraction-ation) process that consists of gene number reduction aft er WGDs

through the removal of the duplicates until the gene content

re-sembles the diploid progenitor genome plus the retained paralogs

( Langham et al., 2004 ; Th

omas et al., 2006 ; Woodhouse et al., 2010 ;

Schnable et al., 2012 ; Murat et al., 2014b ). However, duplicated

gene deletion is not performed at random because it has been

sug-gested that duplicated gene redundancy is eliminated through a

so-called subgenome dominance in which only one of the duplicated

blocks preferentially retains the majority of ancestral copies of the

duplicates. Th

is diploidization phenomenon then leads, at the

whole chromosome or genome levels, to dominant (D, retention of

duplicated genes, also referenced as LF for least fractionated) and

sensitive (S, loss of duplicated genes, also referenced as MF for most

fractionated) subgenomes in paleo- or neopolyploids ( Salse, 2012,

2016 ).

Bias in ancestral gene retention between duplicated blocks

aris-ing from lineage-specifi c polyploidizations has been documented

in Arabidopsis ( Th

omas et al., 2006 ), maize ( Schnable et al., 2011 ),

Brassica ( Cheng et al., 2012 ; Murat et al., 2015 ), and wheat ( Pont

et al., 2013 ). In grasses, this genome fractionation process is clearly

ancestral, as shown in Fig. 3A , in response to shared paleo-WGD

events between ancestral chromosomes A1 and A5, A8 and A9, A2

and A4, A2 and A6, A3 and A7, A3 and A10 ( Schnable et al., 2012 ;

Murat et al., 2014a ). However, an exception to this general

subge-nome dominance pattern has been characterized in cereals where a

highly conserved region has been retained during 50–70 Myr of

evolution between ancestral chromosomes A11–A12 by an active

and recurrent gene conversion phenomenon ( Fig. 3A ) ( Jacquemin

et al., 2011 ; Wang et al., 2011 ).

Investigations of the expressional dynamics of grass duplicates,

deriving form a 90 Myr paleotetraploidization event, suggests that

57.4% ( Yim et al., 2009 ) up to 85% ( Th

roude et al., 2009 ) of the rice

paleoduplicates have diverged in expression. In rice, retained

an-cient gene duplicates associated with high expression tended to

have higher CG body methylation ( Wang et al., 2013 ), suggesting a

direct role of epigenetic regulation in structural and expressional

maintenance of duplicates preventing pseudogenization, silencing

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FIGURE 2 Grass SyntenyViewer tool (adapted from Murat et al., 2014a , b ). Screen capture of the SyntenyViewer web tool (http://urgi.versailles.inra.fr/ synteny) visualizing the synteny between inferred AGK s and modern grass species for applied translational research from model species ( Brachypo-dium ) to crops (wheat, rice, sorghum, maize) or between crops.

and deletion, and ultimately retaining WGD-derived genes. In wheat,

only 28% of the homoeologous triplets, deriving from a

hexaploidi-zation event 0.01–2.5 Ma, have the same expression pattern during

grain development ( Pont et al., 2011 ; Pfeifer et al., 2014 ). Such

mas-sive divergence in expression between duplicates has been

pro-posed as a source of subfunctionalization (partitioning of ancestral

functions between the duplicates, mainly for younger duplicates)

and neofunctionalization (gain of a new nonancestral function of

one duplicate, mainly for old duplicates) of genes during evolution,

both being key forces of evolutionary plasticity in plants ( Zou et al.,

2009 ). Bias in expression abundance between subgenomes

follow-ing duplication has been reported where the D/LF genes harbor

the highest level of expression compared with the S/MF

compart-ment ( Schnable et al., 2011 ; Freeling et al., 2012 ).

Bias in transposable element (TE) content has been also

re-ported between subgenomes in synthetic or naturally occurring

allopolyploids ( Renny-Byfi eld et al., 2011 , 2012 ; Buggs et al., 2012 ),

with the paternal subgenome subject to massive removal of

repeti-tive and nongenic DNA aft er hybridization. Bias in transposable

element (TE) content is not yet confi rmed in paleopolyploids

be-cause the rapid turnover of intergenic repeats makes it diffi

cult

(and in most cases impossible) to detect ancient elements that may

have diff erentially targeted subgenomes that were inherited from

polyploidizations that date back to more than 10 Ma. Transposable

element insertional dynamics may have then participated in the

subgenome restructuring aft er polyploidization so that such

subge-nomes become totally indistinguishable aft er million years of

evo-lution. Th

e insertional activity of TEs may not only drive subgenome

structural diff erentiation, but also the observed epigenetic changes

at the genome-wide and gene-based scales, as one of the

mecha-nisms driving duplicated genes expression partitioning ( Rodin and

Riggs, 2003 ; Rapp and Wendel, 2005 ). It has been reported that

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J U LY 2016 , V O LU M E 103 • S A L S E — PA L E O G E N O M I C S A N D E V O LU T I O N I N G R A S S E S • 1171

FIGURE 3 Evolutionary plasticity following polyploidization (adapted from Murat et al., 2014a ; Salse, 2012 ). (A) Illustration of the subgenome domi-nance after whole-genome duplication in grasses with the average number of ancestral genes (protogenes) retained ( y -axis) in the investigated genomes (species illuminated with a specifi c color code) between duplicated blocks (A1–A5, A8–A9, A11–A12, A2–A4, A2–A6, A3–A7, A3A–10, x -axis), defi ning dominant (D, red circle) and sensitive (S, blue circle) blocks. (B) Schematic illustration of the biased structural and expressional genome par-titioning following polyploidization in plants acting as a source of genomic plasticity in modern species. Genes are illustrated as colored boxes, deleted genes with red crosses, and expression modifi cation as a theoretical expression pattern during development. TE, transposable element.

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dominantly expressed genes in D/LF subgenomes have fewer 24-bp

RNA-targeted TEs in their 1-kb fl anking regions compared with

their S/MF paralogs ( Woodhouse et al., 2014 ), with small

RNA-targeted TEs shown to be subject to methylation, potentially

sup-pressing nearby gene expression ( Hollister and Gaut, 2009 ). All

these observations may suggest that diff erences in TE content and

insertional dynamics either between prepolyploidization progenitors

(in the case of allopolyploidy, merging paternal/maternal genomes

from distinct species) and/or between the postpolyploidization

subgenomes (in the case of autopolyploidy, doubling genomes from

the same species) may drive (small RNA-targeted) TE-mediated

epigenetic changes in promoting gene neo- or

subfunctionaliza-tion, silencing and ultimately deletion following polyploidizasubfunctionaliza-tion,

leading to the observed biased fractionation between D/LF and S/

MF compartments. However, this postpolyploidy structural and

functional plasticity driven by subgenomic dominance seems to

re-quire some time to “evolve” and “stabilize” as proposed from

stud-ies on resynthesized polyploids ( Renny-Byfi eld et al., 2015 ).

Despite this general phenomenon of massive and biased DNA

loss (including duplicates) following WGDs, ancestral genes can be

retained as pairs (referred to as Ohnologs; Ohno, 1970 ) during

evo-lution. Th

ese genes that survive diploidization (or

“diploidization-resistant” genes) are enriched in functional annotations such as

transcription factor, transcription regulator, and ribosomal protein

gene ( Freeling, 2009 ). Several hypotheses (probably interconnected

ones) have been proposed to explain duplicated gene retention such

as at (1) the function level with the acquisition of novel function

(neo- and subfunctionalization; Lynch and Conery, 2000 ; Wang

et al., 2012 ), (2) the network level with the maintenance of a

stoi-chiometric balance of gene product interactions (or connectivity)

in macromolecular complexes ( Birchler and Veitia, 2011 , 2014 ),

(3) the phenotypic level with a heterotic eff ect with transgressive

performances ( Birchler et al., 2010 ), (4) the allelic level in masking

deleterious recessive mutations ( Gu, 2003 ), (5) the adaptation level

with escape from adaptative confl icts ( Des Marais and Rausher,

2008 ), (6) the expression level with a higher level of expression

as-sociated with higher CG gene body methylation (

Seoighe and

Wolfe, 1999 ; Aury et al., 2006 ; Yang and Gaut, 2011 ), all potentially

delivering to the newly formed polyploid a machinery absent from

the diploid progenitors. It has been reported that such retained

du-plicated genes in rice are enriched in single nucleotide

polymor-phisms (SNPs) encoding less radical amino acid changes, suggesting

that such “advantageous” material/genes inherited from WGDs are

highly stable (i.e., slow rate of evolution) over the time ( Chapman

et al., 2006 ).

Overall, such structural (chromosome fusion/fi ssion/translocation,

gene/DNA loss, TE dynamics) and functional (neo- and

subfunc-tionalization, expression, network connectivity) partitioning of the

subgenomes following polyploidization participate in

homoeolo-gous chromosome (subgenomes) diff erentiation, then (1)

stabiliz-ing meiotic pairstabiliz-ing by preventstabiliz-ing chromosome pairstabiliz-ing while

increasing fertility of the nascent postpolyploidy lineages distinctly

diff erent from their ancestral progenitors and (2) ultimately

pro-vide genetic material to be “specialized” for key innovations such as

phenotypic novelty, altogether being potentially responsible for the

evolutionary success of polyploidy plants and novel desirable traits

selected during domestication by humans ( Fig. 3B ). For example,

nascent hexaploid wheat has been shown to exhibit hybrid vigor

and adaptive traits (such as robust seedling growth, larger spikes

with longer rachis internodes, and salt tolerance) when compared

with their parents ( He et al., 2003 ; Colmer et al., 2006 ; Yang et al.,

2014 ). Beside the knowledge gained during the last decade on the

role of polyploidy in plant species evolution and adaptation, still a

lot needs to be achieved and investigated to precisely characterize

the driving molecular mechanisms and so that they can be used in

breeding.

CONCLUSION

Overall, the consequences of polyploidization (reshaping gene

con-tent, expression, functions, TE compartment, CG gene body

meth-ylation) could explain how WGDs may have favored the emergence

of new plant species during the last 300 Myr of evolution. Such

evo-lutionary plasticity gained from polyploidization events provides

the basis for functional and phenotypic novelty in angiosperms.

Such novelty may fi nally be achieved through duplicate-based

functional divergence, gene conversion, changes in expression,

dosage eff ects, and network specialization and may ultimately

un-derlie the observed evolutionary success of angiosperms. However,

the continuum and interplay between the reported structural and

functional reprogramming aft er polyploidization are still poorly

understood. Synthetic polyploids may further expand our nascent

knowledge about this major phenomenon driving plant

evolution-ary dynamics.

ACKNOWLEDGEMENTS

Th

is work has been supported by grants from the Agence Nationale

de la Recherche (ANR Blanc-PAGE, ref : ANR-2011-BSV6-00801).

Th

e author thanks Caroline Pont and Florent Murat for their

participation in formatting the illustrations.

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