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Current Plant Biology 1 (2014) 34–39

Contents lists available at ScienceDirect

Current Plant Biology

jo u r nal homep age: www.elsev ier .com/ locate /cpb

aleogenomics in Triticeae for translational research

lorent Murat1, Caroline Pont1, Jérôme Salse ∗

NRA/UBP UMR 1095 GDEC ‘Génétique, Diversité et Ecophysiologie des Céréales’, 5 Chemin de Beaulieu, 63100 Clermont Ferrand, France

r t i c l e i n f o

rticle history:eceived 30 April 2014eceived in revised form 25 August 2014ccepted 25 August 2014

a b s t r a c t

Recent access to Triticeae genome sequences as well as high resolution gene-based genetic maps recentlyoffered the opportunity to compare modern Triticeae genomes and model their evolutionary history fromtheir reconstructed founder ancestors. In silico paleogenomic data have revealed the evolutionary forcesthat have shaped present-day Triticeae and allowed to gain insight into how wheat, barley, rye genomesare organized today compared to their grass relatives (rice, sorghum, millet and maize).

eywords:riticeaeyntenyuplicationvolutionenome

© 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/3.0/).

ncestor

ontents

1. Triticeae genome evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 342. Triticeae genome partitioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363. Wheat genome partitioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 364. Translational research in Triticeae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39

. Triticeae genome evolution

Based on the BLAST-derived orthologous relationships and usingRIMM-synteny [1] to define syntenic groups as well as ANGES

2] to define ancestral gene order, the grasses has been proposedo derive from AGK (Ancestral Grass Karyotype) structured in

= 7 protochromosomes (or CARs for Conserved Ancestral Regions)ontaining 8581 ordered protogenes, dating back to 90 millionears ago (hereafter mya), Fig. 1 [3]. In this scenario grasseserived from this n = 7 ancestor that went through a whole genome

A2-A4-A6 and A3-A7-A10 protochromosomes, black arrows Fig. 1),three inversions (in A5/A3 and A2 protochromosomes) as wellas two translocations (between A4-A8 and A3-A12 protochro-mosomes) to reach a n = 12 AGK post-duplication intermediatecontaining 16464 protogenes (Fig. 1) [3]. Modern grass (maize, mil-let and sorghum) genomes were proposed to have derived fromthis duplicated intermediate (i.e. their genome consists then in amosaic of A1-A5, A2-A4, A2-A6, A3-A7, A3-A10, A8-A9, A11-A12paralogous ancestral blocks) through distinct ancestral chromo-some fusion patterns. The modern rice genome [4] has retained

uplication (hereafter WGD, R for ‘round’ of WGD) to reach a = 14 (A1-A14 CARs) AGK intermediate, Fig. 1. Ancestral small-cale shuffling events took place between the duplicated blocks inhe n = 14 AGK with two telomeric/centromeric fusions (involving

∗ Corresponding author. Tel.: +33 0473624380; fax: +33 0473624453.E-mail addresses: florent.murat@clermont.inra.fr (F. Murat),

aroline.pont@clermont.inra.fr (C. Pont), jsalse@clermont.inra.fr (J. Salse).1 These authors equally contributed to the work.

ttp://dx.doi.org/10.1016/j.cpb.2014.08.003214-6628/© 2014 The Authors. Published by Elsevier B.V. This is an open access article un

the chromosome number of 12, derived from the post-duplicationn = 12 AGK intermediate, making this genome as a reference kar-yotype for comparative genomics investigation in grasses (Fig. 1)[3].

The development of NGS (next generation sequencing)approaches and technologies (Solexa, SOLid, 454) allowed high-throughput WGS (whole genome shotgun) based sequencing of

both simple and complex (i.e. high repeat content as well aspolyploid) genomes. Table 1 provides information regarding theTriticeae genomes and sequence-based genetic maps available to

der the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

F. Murat et al. / Current Plant Biology 1 (2014) 34–39 35

Fig. 1. Triticeae genome paleohistory scenario. The present-day Triticeae genomes (bottom) are represented with color codes to illuminate the evolution of segments fromtheir founder ancestors (top) with seven protochromosomes (referenced as AGK and ATK). WGD events that have shaped the structure of the different Triticeae genomesduring their evolution from their common ancestors are indicated in red (i.e. 1R, 2R and 3R). Evolutionary genome shuffling events such as chromosomal fusions andtranslocations are indicated in boxes with black arrows. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of thearticle.)

Table 1Triticeae genome data sets used in paleogenomics studies.

Species Name Chr Size (Mbp) TE (%) Mapped genes/markers Syntenic genes Chr. equation WGD

Reference Oryza sativa Rice 12 372/39 41046 [4] RG 2 × 7 − 2 1ROutgroup Lolium perenne Ryegrass 7 2600/>80 762 [10] 84 2 × 7 − 2 + 1 − 6 1R

Triticum aestivum Wheat 21 ∼17,000/>80 40267 [9]/124201 [15] 24725 (2 × 7 − 2 + 1 − 6) × 3 3RTriticeae Hordeum vulgare Barley 7 ∼5000/>80 15719 [6] 5430 2 × 7 − 2 + 1 − 6 1R

Secale cereale Rye 7 7917/>80 2940 [8] 1205 2 × 7 − 2 + 1 − 6 1R

RG refers to Reference Genome indicating that rice has been used as reference genome for the paleogenomics analysis of Triticeae genomes.

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ate in the public domain for paleogenomics investigation. TheTK (for Ancestral Triticeae Karyotype) have been then proposed toave derived from the n = 12 AGK through 4 centromeric ancestralhromosome fusions (leading to functional monocentric neochro-osomes), 1 fission and 2 telomeric ancestral chromosome fusions,

nvolving, with T for ancestral Triticeae chromosomes, the follow-ng chromosome relationships: T1 = A10 + A5, T2 = A7 + A4, T3 = A1,4 = A11 + A3, T5 = A9 + A12, T6 = A2, T7 = A8 + A6, Fig. 1 [5]. Overall,he paleohistory of modern Triticeae genomes from the recon-tructed AGK paleokaryotypes involves numerous WGD events1R-3R) as well as ancestral chromosome fusion (−6 in the equa-ion) and fission (+1 in the equation) events according to theetailed karyotypic equations provided in Table 1. The modernarley genome (Hordeum vulgare, 15719 mapped genes associatedith 5430 rice orthologs) has retained the original ATK chromo-

ome number of 7, making this genome as a reference karyotypeor comparative genomics investigation within the Triticeae tribe6,7]. Based on 2940 mapped genes associated with 1205 orthologs,he modern rye (Secale cereale) genome derived from the n = 7TK followed by an ancestral reciprocal translocation (between4 and A5) plus 5 lineage-specific translocations (between A3-A6,6-A7, A4-A7, A2-A7 and A4-A6) [8]. The modern bread wheatenome (Triticum aestivum, 40267 mapped genes with 24725rthologs) shares the ancestral reciprocal translocation (between4-A5 on the A subgenome) characterized in rye and underwent

wo hybridization events (2R, 3R) between A, B and D progenitorssee Section 2) as well as an additional lineage-specific transloca-ion (between 4A and 7B) to reach the modern 21 chromosomes [5].nterestingly, ryegrass (Lolium perenne, 762 mapped genes with 84rthologs), that is not a Triticeae, presents a modern karyotype of

chromosomes close to ATK, suggesting that this ancestral Trit-ceae genome structure is older than the pure datation based onhe speciation of the modern Triticeae, i.e. 13 mya [9].

. Triticeae genome partitioning

According to the previous evolutionary scenario, Triticeaeenomes have been duplicated at least once in the course of theiraleohistory. Such polyploidization constitutes a genomic shocknd leads to a diploidization process where duplicated genes areost by massive local deletions. However, duplicated gene dele-ion is not performed at random at the genome level as it haseen suggested that duplicate gene redundancy is eliminatedhrough a so-called subgenome dominance in which only one ofhe duplicated blocks retain the majority of ancestral copies of theuplicates. Bias in duplicated gene deletion has been described only

n a few grass genomes or gene families [10–13].The precise characterization of ancestral duplicates that are

aintained at syntenic locations in modern grass genomes andf duplicates that have been deleted/shuffled allowed to preciselydentify shared Dominant (D, preferential retention of ancestralenes) and Sensitive (S, enhanced deletion of ancestral genes)ubgenomes in modern grasses [3]. The analysis of the fate ofncestral duplicates clearly established that in the n = 12 AGK inter-ediate (also exemplified by rice as the modern representative

f AGK), A1-2-3-4-9-11 are dominant genomic compartments and5-6-7-8-10-12 are sensitive ones (cf D and S blocks in Fig. 1, AGKnd rice panels). It cannot be excluded that the established bias inene content reflecting ancestral subgenome dominance in grassesay be considered as an evidence that the ancestral grass duplica-

ion resulted from an allotetraploidy event between structurally

ontrasted progenitor 1 (A5-A6-A7-A8-A10-A12) and progenitor 2A1-A2-A3–A4-A9-A11) [3].

Following this scenario of subgenome dominance, modernriticeae karyotypes should also consist in D and S fragments

Biology 1 (2014) 34–39

inherited from the ancestral WGD. The previously describedchromosome-to-chromosome relationships between rice and Trit-iceae (see Section 1), allowed to transfer the ancestral dominant(A1-2-3-4-9-11, associated with higher retention of ancestralgenes) and sensitive (A5-6-7-8-10-12, associated with enhancedloss of ancestral genes) chromosomal blocks reported in grassesinto the 7 ATK chromosomes (Fig. 1 with D and S blocks in ATKpanel) so that any modern Triticeae can then be re-organizedinto paleo-D and paleo-S (i.e. paralogous Dominant (D) and Sen-sitive (S) blocks deriving from the ancestral WGD) chromosomalcompartments where T1(S) = A10(S) + A5(S), T2(D) = A7(S) + A4(D),T3(D) = A1(D), T4(D) = A11(D) + A3(D), T5(D) = A9(D) + A12(S),T6(D) = A2(D), T7(S) = A8(S) + A6(S), (cf D and S blocks in Fig. 1, ATKpanel). This phenomenon may have participated into the reporter‘reticulate evolution’ of the Triticeae genomes and particularly inrye where asymmetric conserved syntenic gene content betweenchromosomal segments has been documented [8].

3. Wheat genome partitioning

Bread wheat derived from the AGK structured in 7 protochromo-somes followed by a paleotetraploidization (1R in Fig. 1, leading topairs of dominant and sensitive chromosomes) to reach a 12 chro-mosomes AGK intermediate with 6 ancestral chromosome fusionsand one fission to reach the ATK followed by a neohexaploidiza-tion (involving progenitors/subgenomes A, B and D) event (2R, 3Rin Fig. 1 dating back respectively to 0.5 and 0.1 mya) that finallyshaped the 21 modern chromosomes. Wheat genomics resourceshave been recently published with the release of the wheatgenome shotgun sequences in hexaploid [14,15] and diploids (i.e.D genome ancestor [16,17] as well as the A genome progenitor[18] sequences). Moreover, genome-wide diversity maps have beenalso made recently available in hexaploids [19], tetraploids [20]or diploid progenitors [21]. Structural dissymmetry between thewheat subgenomes have been documented in the literature, basedon cytology [22], nuclear [23] or mitochondrial DNA sequences [24],large-scale structural changes such as translocation events [25] andmolecular markers (SSRs [26], RFLPs [27] and SNPs [28,29]), thenopening the question of the phylogenetic history of the bread wheatgenome from its founder ancestors Triticum urartu (A subgenome)and Aegilops speltoides (B subgenome) and Aegilops tauschii (Dsubgenome).

The structural dissymmetry between B subgenome and A. spel-toides compared to A subgenome/T. urartu and D subgenome/A.tauschii was classically explained with an hypothesis relying onthe controversial B genome origin where either (i) its progenitoris a unique Aegilops species that remains unknown (i.e. mono-phyletic origin and ancestor closely related to A. speltoides fromthe Sitopsis section) or (ii) this genome resulted from an introgres-sion of several parental Aegilops species (i.e. polyphyletic origin)that need to be identified from the Sitopsis section [23]. The asym-metric genomic and genetic plasticity between the modern wheatsubgenomes have then been tentatively explained so far throughthe previous hypothesis relying purely on different mating systemsof the diploid progenitors (cross-pollinating progenitors for B andself-pollinating progenitors for A and D) also associated with theassumption of a constant and similar evolutionary rate betweensubgenomes after polyploidization (i.e. tetraploidy A vs. B andhexaploidy AB vs. D), Fig. 2 (scenario #1 referenced as ‘B /= (A − D)’).

Alternatively, based on sequence evidences in wheat of 5234ancestral grass genes, we proposed that the subgenome dominance

phenomenon following the ancestral shared paleotetraploidiza-tion event (1R), as reported in the previous section, may alsoacts between the A, B and D subgenomes deriving form theneohexaploidization then explaining the observed contrasted

F. Murat et al. / Current Plant Biology 1 (2014) 34–39 37

Fig. 2. Wheat genome paleohistory scenario. LEFT – Scenario #1 represents the origin of the contrasted evolutionary plasticity of subgenomes B-A-D through diploid matingsystem differences, i.e. pre-polyploidization hypothesis. MIDDLE – Scenario #2 represents the origin of the evolutionary plasticity of subgenomes B-A-D through differentialcontrasted modes of evolution between dominant (D, in blue) and sensitive (S, in red) blocks, i.e. post-polyploidization hypothesis. RIGHT – Scenario #3 represents the origino D subfi

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f the evolutionary plasticity of subgenomes B-A-D through the hybrid origin of thegure legend, the reader is referred to the web version of the article.)

heat subgenomic plasticity (Fig. 2, scenario #2 referenced as > A > D). We then proposed an evolutionary scenario where theodern bread wheat genome has been shaped through a first

eotetraploidization event (0.5 mya) leading to a subgenome dom-nance where the A subgenome was dominant (i.e. stable) andhe B subgenome sensitive (i.e. plastic); while the second neo-exaploidization event (0.1 mya) leaded to a supra-dominancehere the tetraploid became sensitive (subgenomes A and B) and

he D subgenome supradominant (i.e. pivotal) [30]. Thus, the mod-rn bread wheat genome can be divided into five supra-dominanthromosomes (also referenced as pivotal) deriving from surim-osed dominances (i.e. chromosomes 3D, 2D-S/L, 4D, 5D-L, 6D-S/L)

n contrast to five supra-sensitive ones (i.e. chromosomes 1B, 2B-, 5B-S, 6B-C, 7B), and the remaining regions are associated withpposite D and S effects following the successive duplication eventsi.e. with S for short arm, L for long arm and C for centromeric region)30].

Recently, a third scenario have been proposed suggesting thathe gene content of A and B subgenomes is more similar to Dhan to each other at the whole chromosome level and at theene sequence relatedness [15,31]. Based on 275 reconstructedene trees between hexaploid and diploid wheat species, show-ng that A and B subgenomes are more similar to the D individuallyhan they are to each other, the authors proposed that the bread

heat genome has been shaped through two rounds of hybridiza-

ion between A and B genomes, giving rise to the D genome [31].n this scenario the hybrid origin of the D lineage deriving from anqual contribution of the A and B lineages may explain the reported

genome from A and B lineages. (For interpretation of the references to color in this

contrasted genomic plasticity between the wheat subgenomes(Fig. 2, scenario #3 referenced as ‘(B − A) → D’).

All the proposed scenarios aiming at explaining the struc-tural asymmetry characterized between the wheat subgenomesneed to be now considered and validated at the wholegenome scale and multi-species/lineages investigation, i.e. eithera pre-polyploidization mechanism where the evolutionary his-tory of the cross-pollinator A. speltoides progenitor (B donor)had a more diverse genome that self-pollinators T. urartu/A.tauschii (A/D donors), scenario #1 referenced as ‘B /= (A − D)’; apost-polyploidization mechanism with an accelerated structuralplasticity on 10 sensitive compartments in contrast to 10 stablecounterparts following the subgenome dominance phenomenon,scenario #2 referenced as ‘B > A > D’; and finally an hybrid originof the D lineage from A and B lineages, scenario #3 referenced as‘(B − A) → D’.

4. Translational research in Triticeae

Paleogenomic data and derived modern karyotype orga-nizations, illustrated as a mosaic of reconstructed ancestralprotochromosome (either AGK or ATK segments, Fig. 1), allowedthe presentation of modern Triticeae chromosomes as crop circles[32] as refinement of the model initially proposed in the 90s forthe grasses by Mike Gale’s group [33]. Fig. 3 (top) shows the ‘Trit-

iceae syntenome circles’ involving three Triticeae species of majoragronomic interest, wheat–barley–rye. For any radius of the circlesa translational genomics approach can be accurately applied in (i)

38 F. Murat et al. / Current Plant Biology 1 (2014) 34–39

Fig. 3. Triticeae syntenome circles. TOP – The center of the circle illustrates the Triticeae chromosomes origin from ATK (Ancestral Triticeae Karyotype) structured in 7protochromosomes (color code, right), with barley (inner circle referenced as ‘Hv’ circle for Hordeum vulgare) as its modern representative. The external concentric circlesillustrate the 7 chromosomes of rye (referenced as ‘Sc’ circle for S. cereale) as well as the 21 bread wheat chromosomes (referenced ‘TaA’, ‘TaB’ and ‘TaD’ circles for Triticuma colorew een A( s figur

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estivum subgenomes A, B and D) based on the sequenced/mapped gene orthologs (eb tool [http://urgi.versailles.inra.fr/synteny-wheat] visualizing the synteny betw

ID, primer pairs, SNP in wheat). (For interpretation of the references to color in thi

arker development, (ii) improving conserved gene annotation oriii) candidate gene selection for traits of interest (either conservedr lineage-specific ones) [34].

Such high resolution and large-scale comparative genomicsnformation offer a tremendous set of gene-based markers thatan be used directly as founder resource for genome mapping and

ltimately trait dissection. Regarding the synteny-based selectionf genic markers, the robust identification of collinear regions (i.e.adius of the syntenome circles) delivered 16464 COS (conservedrthologous set) markers for SNP discovery in grasses [30,35]. Such

d vertical bars on the circles). BOTTOM – Screen capture of the PlantSyntenyViewerTK, Brachypodium, rice, maize, sorghum and providing the COS gene informatione legend, the reader is referred to the web version of the article.)

resolution of synteny-based COS markers has been used in wheat (i)to refine metaQTL intervals and immediately benefit from the COSmarkers to access robust links with sequence genomes and preciseorthologous candidate genes as illustrated for nitrogen use effi-ciency [36], grain fiber content [37], carotenoid content [38] traits,and (ii) as a matrix for physical map construction [39].

Overall, the Triticeae syntenome and more generally the grasssyntenome, delivered through a public web interface PlantSyn-tenyViewer at http://urgi.versailles.inra.fr/synteny-wheat, can beconsidered as a guide for accelerated dissection of major

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gronomical traits in wheat [30,34]. Fig. 3 illustrates the PlantSyn-enyViewer tool delivering for any of the 7 ATK protochromosomesrecise orthologous relationships with rice, maize, sorghum andrachypodium as a source of markers or candidate genes.

Besides, structural comparisons of the grasses and morearticularly the Triticeae genomes, integration of NGS-basedranscriptome and methylome data in the provided Triticeae syn-enome system will allow to address in the future not only thevolutionary trends of genes or chromosome architectures but alsoheir expression and epigenetic landscapes. It will then be possibleo investigate the impact of the reported evolutionary asymme-ry between the wheat subgenome structures (i.e. three proposedcenarios) onto expressional and epigenetic differences betweenomoeologs.

cknowledgment

This work has been supported by grants from the Agenceationale de la Recherche (program ANR Blanc-PAGE, ref: ANR-011-BSV6-00801).

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