Paleogenomics in Triticeae for Translational Research

Current Plant Biology 1 (2014) 34–39

Contents lists available at ScienceDirect

Current Plant Biology

jo urnal homepage: www.elsevier.com/locate/cpb

Paleogenomics in Triticeae for translational research

1 1 ∗

Florent Murat , Caroline Pont , Jérôme Salse

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

a r t i c l e i n f o a b s t r a c t

Article history: Recent access to Triticeae genome sequences as well as high resolution gene-based genetic maps recently

Received 30 April 2014

offered the opportunity to compare modern Triticeae genomes and model their evolutionary history from

Received in revised form 25 August 2014

their reconstructed founder ancestors. In silico paleogenomic data have revealed the evolutionary forces

Accepted 25 August 2014

that have shaped present-day Triticeae and allowed to gain insight into how wheat, barley, rye genomes

are organized today compared to their grass relatives (rice, sorghum, millet and maize).

Keywords:

license (http://creativecommons.org/licenses/by-nc-nd/3.0/). Synteny Duplication Evolution Genome Ancestor

Contents

1. Triticeae genome evolution ...... 34

2. Triticeae genome partitioning ...... 36

3. Wheat genome partitioning ...... 36

4. Translational research in Triticeae ...... 37

Acknowledgment...... 39

References ...... 39

1. Triticeae genome evolution A2-A4-A6 and A3-A7-A10 protochromosomes, black arrows Fig. 1),

three inversions (in A5/A3 and A2 protochromosomes) as well

Based on the BLAST-derived orthologous relationships and using as two translocations (between A4-A8 and A3-A12 protochro-

DRIMM-synteny [1] to deﬁne syntenic groups as well as ANGES mosomes) to reach a n = 12 AGK post-duplication intermediate

[2] to deﬁne ancestral gene order, the grasses has been proposed containing 16464 protogenes (Fig. 1) [3]. Modern grass (maize, mil-

to derive from AGK (Ancestral Grass Karyotype) structured in let and sorghum) genomes were proposed to have derived from

n = 7 protochromosomes (or CARs for Conserved Ancestral Regions) this duplicated intermediate (i.e. their genome consists then in a

containing 8581 ordered protogenes, dating back to 90 million mosaic of A1-A5, A2-A4, A2-A6, A3-A7, A3-A10, A8-A9, A11-A12

years ago (hereafter mya), Fig. 1 [3]. In this scenario grasses paralogous ancestral blocks) through distinct ancestral chromo-

derived from this n = 7 ancestor that went through a whole genome some fusion patterns. The modern rice genome [4] has retained

duplication (hereafter WGD, R for ‘round’ of WGD) to reach a the chromosome number of 12, derived from the post-duplication

n = 14 (A1-A14 CARs) AGK intermediate, Fig. 1. Ancestral small- n = 12 AGK intermediate, making this genome as a reference kar-

scale shufﬂing events took place between the duplicated blocks in yotype for comparative genomics investigation in grasses (Fig. 1)

the n = 14 AGK with two telomeric/centromeric fusions (involving [3].

The development of NGS (next generation sequencing)

approaches and technologies (Solexa, SOLid, 454) allowed high-

∗ throughput WGS (whole genome shotgun) based sequencing of

Corresponding author. Tel.: +33 0473624380; fax: +33 0473624453.

both simple and complex (i.e. high repeat content as well as

E-mail addresses: ﬂ[email protected] (F. Murat),

polyploid) genomes. Table 1 provides information regarding the

[email protected] (C. Pont), [email protected] (J. Salse).

These authors equally contributed to the work. Triticeae genomes and sequence-based genetic maps available to

http://dx.doi.org/10.1016/j.cpb.2014.08.003

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 from

their founder ancestors (top) with seven protochromosomes (referenced as AGK and ATK). WGD events that have shaped the structure of the different Triticeae genomes

during their evolution from their common ancestors are indicated in red (i.e. 1R, 2R and 3R). Evolutionary genome shufﬂing events such as chromosomal fusions and

translocations 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 the article.)

Table 1

Triticeae 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 1R

Outgroup 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 3R

Triticeae 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.

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

date in the public domain for paleogenomics investigation. The inherited from the ancestral WGD. The previously described

ATK (for Ancestral Triticeae Karyotype) have been then proposed to chromosome-to-chromosome relationships between rice and Trit-

have derived from the n = 12 AGK through 4 centromeric ancestral iceae (see Section 1), allowed to transfer the ancestral dominant

chromosome fusions (leading to functional monocentric neochro- (A1-2-3-4-9-11, associated with higher retention of ancestral

mosomes), 1 ﬁssion and 2 telomeric ancestral chromosome fusions, genes) and sensitive (A5-6-7-8-10-12, associated with enhanced

involving, with T for ancestral Triticeae chromosomes, the follow- loss of ancestral genes) chromosomal blocks reported in grasses

ing chromosome relationships: T1 = A10 + A5, T2 = A7 + A4, T3 = A1, into the 7 ATK chromosomes (Fig. 1 with D and S blocks in ATK

T4 = A11 + A3, T5 = A9 + A12, T6 = A2, T7 = A8 + A6, Fig. 1 [5]. Overall, panel) so that any modern Triticeae can then be re-organized

the paleohistory of modern Triticeae genomes from the recon- into paleo-D and paleo-S (i.e. paralogous Dominant (D) and Sen-

structed AGK paleokaryotypes involves numerous WGD events sitive (S) blocks deriving from the ancestral WGD) chromosomal

(1R-3R) as well as ancestral chromosome fusion (−6 in the equa- compartments where T1(S) = A10(S) + A5(S), T2(D) = A7(S) + A4(D),

tion) and ﬁssion (+1 in the equation) events according to the T3(D) = A1(D), T4(D) = A11(D) + A3(D), T5(D) = A9(D) + A12(S),

detailed karyotypic equations provided in Table 1. The modern T6(D) = A2(D), T7(S) = A8(S) + A6(S), (cf D and S blocks in Fig. 1, ATK

barley genome (Hordeum vulgare, 15719 mapped genes associated panel). This phenomenon may have participated into the reporter

with 5430 rice orthologs) has retained the original ATK chromo- ‘reticulate evolution’ of the Triticeae genomes and particularly in

some number of 7, making this genome as a reference karyotype rye where asymmetric conserved syntenic gene content between

for comparative genomics investigation within the Triticeae tribe chromosomal segments has been documented [8].

[6,7]. Based on 2940 mapped genes associated with 1205 orthologs,

the modern rye (Secale cereale) genome derived from the n = 7

ATK followed by an ancestral reciprocal translocation (between 3. Wheat genome partitioning

A4 and A5) plus 5 lineage-speciﬁc translocations (between A3-A6,

A6-A7, A4-A7, A2-A7 and A4-A6) [8]. The modern bread wheat Bread wheat derived from the AGK structured in 7 protochromo-

genome (Triticum aestivum, 40267 mapped genes with 24725 somes followed by a paleotetraploidization (1R in Fig. 1, leading to

orthologs) shares the ancestral reciprocal translocation (between pairs of dominant and sensitive chromosomes) to reach a 12 chro-

A4-A5 on the A subgenome) characterized in rye and underwent mosomes AGK intermediate with 6 ancestral chromosome fusions

two hybridization events (2R, 3R) between A, B and D progenitors and one ﬁssion to reach the ATK followed by a neohexaploidiza-

(see Section 2) as well as an additional lineage-speciﬁc translocation (involving progenitors/subgenomes A, B and D) event (2R, 3R

tion (between 4A and 7B) to reach the modern 21 chromosomes [5]. in Fig. 1 dating back respectively to 0.5 and 0.1 mya) that ﬁnally

Interestingly, ryegrass (Lolium perenne, 762 mapped genes with 84 shaped the 21 modern chromosomes. Wheat genomics resources

orthologs), that is not a Triticeae, presents a modern karyotype of have been recently published with the release of the wheat

7 chromosomes close to ATK, suggesting that this ancestral Trit- genome shotgun sequences in hexaploid [14,15] and diploids (i.e.

iceae genome structure is older than the pure datation based on D genome ancestor [16,17] as well as the A genome progenitor

the speciation of the modern Triticeae, i.e. 13 mya [9]. [18] sequences). Moreover, genome-wide diversity maps have been

also made recently available in hexaploids [19], tetraploids [20]

or diploid progenitors [21]. Structural dissymmetry between the

2. Triticeae genome partitioning wheat subgenomes have been documented in the literature, based

on cytology [22], nuclear [23] or mitochondrial DNA sequences [24],

According to the previous evolutionary scenario, Triticeae large-scale structural changes such as translocation events [25] and

genomes have been duplicated at least once in the course of their molecular markers (SSRs [26], RFLPs [27] and SNPs [28,29]), then

paleohistory. Such polyploidization constitutes a genomic shock opening the question of the phylogenetic history of the bread wheat

and leads to a diploidization process where duplicated genes are genome from its founder ancestors Triticum urartu (A subgenome)

lost by massive local deletions. However, duplicated gene dele- and Aegilops speltoides (B subgenome) and Aegilops tauschii (D

tion is not performed at random at the genome level as it has subgenome).

been suggested that duplicate gene redundancy is eliminated The structural dissymmetry between B subgenome and A. spel-

through a so-called subgenome dominance in which only one of toides compared to A subgenome/T. urartu and D subgenome/A.

the duplicated blocks retain the majority of ancestral copies of the tauschii was classically explained with an hypothesis relying on

duplicates. Bias in duplicated gene deletion has been described only the controversial B genome origin where either (i) its progenitor

in a few grass genomes or gene families [10–13]. is a unique Aegilops species that remains unknown (i.e. mono-

The precise characterization of ancestral duplicates that are phyletic origin and ancestor closely related to A. speltoides from

maintained at syntenic locations in modern grass genomes and the Sitopsis section) or (ii) this genome resulted from an introgres-

of duplicates that have been deleted/shufﬂed allowed to precisely sion of several parental Aegilops species (i.e. polyphyletic origin)

identify shared Dominant (D, preferential retention of ancestral that need to be identiﬁed from the Sitopsis section [23]. The asym-

genes) and Sensitive (S, enhanced deletion of ancestral genes) metric genomic and genetic plasticity between the modern wheat

subgenomes in modern grasses [3]. The analysis of the fate of subgenomes have then been tentatively explained so far through

ancestral duplicates clearly established that in the n = 12 AGK inter- the previous hypothesis relying purely on different mating systems

mediate (also exempliﬁed by rice as the modern representative of the diploid progenitors (cross-pollinating progenitors for B and

of AGK), A1-2-3-4-9-11 are dominant genomic compartments and self-pollinating progenitors for A and D) also associated with the

A5-6-7-8-10-12 are sensitive ones (cf D and S blocks in Fig. 1, AGK assumption of a constant and similar evolutionary rate between

and rice panels). It cannot be excluded that the established bias in subgenomes after polyploidization (i.e. tetraploidy A vs. B and

gene content reﬂecting ancestral subgenome dominance in grasses hexaploidy AB vs. D), Fig. 2 (scenario #1 referenced as ‘B =/ (A − D)’).

may be considered as an evidence that the ancestral grass duplica- Alternatively, based on sequence evidences in wheat of 5234

tion resulted from an allotetraploidy event between structurally ancestral grass genes, we proposed that the subgenome dominance

contrasted progenitor 1 (A5-A6-A7-A8-A10-A12) and progenitor 2 phenomenon following the ancestral shared paleotetraploidiza-

(A1-A2-A3–A4-A9-A11) [3]. tion event (1R), as reported in the previous section, may also

Following this scenario of subgenome dominance, modern acts between the A, B and D subgenomes deriving form the

Triticeae karyotypes should also consist in D and S fragments neohexaploidization 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 mating

system differences, i.e. pre-polyploidization hypothesis. MIDDLE – Scenario #2 represents the origin of the evolutionary plasticity of subgenomes B-A-D through differential

contrasted modes of evolution between dominant (D, in blue) and sensitive (S, in red) blocks, i.e. post-polyploidization hypothesis. RIGHT – Scenario #3 represents the origin

of the evolutionary plasticity of subgenomes B-A-D through the hybrid origin of the D subgenome from A and B lineages. (For interpretation of the references to color in this

ﬁgure legend, the reader is referred to the web version of the article.)

wheat subgenomic plasticity (Fig. 2, scenario #2 referenced as contrasted genomic plasticity between the wheat subgenomes

B > A > D). We then proposed an evolutionary scenario where the (Fig. 2, scenario #3 referenced as ‘(B − A) → D’).

modern bread wheat genome has been shaped through a ﬁrst All the proposed scenarios aiming at explaining the struc-

neotetraploidization event (0.5 mya) leading to a subgenome dom- tural asymmetry characterized between the wheat subgenomes

inance where the A subgenome was dominant (i.e. stable) and need to be now considered and validated at the whole

the B subgenome sensitive (i.e. plastic); while the second neo- genome scale and multi-species/lineages investigation, i.e. either

hexaploidization event (0.1 mya) leaded to a supra-dominance a pre-polyploidization mechanism where the evolutionary his-

where the tetraploid became sensitive (subgenomes A and B) and tory of the cross-pollinator A. speltoides progenitor (B donor)

the D subgenome supradominant (i.e. pivotal) [30]. Thus, the mod- had a more diverse genome that self-pollinators T. urartu/A.

ern bread wheat genome can be divided into ﬁve supra-dominant tauschii (A/D donors), scenario #1 referenced as ‘B =/ (A − D)’; a

chromosomes (also referenced as pivotal) deriving from surim- post-polyploidization mechanism with an accelerated structural

posed dominances (i.e. chromosomes 3D, 2D-S/L, 4D, 5D-L, 6D-S/L) plasticity on 10 sensitive compartments in contrast to 10 stable

in contrast to ﬁve supra-sensitive ones (i.e. chromosomes 1B, 2B- counterparts following the subgenome dominance phenomenon,

C, 5B-S, 6B-C, 7B), and the remaining regions are associated with scenario #2 referenced as ‘B > A > D’; and ﬁnally an hybrid origin

opposite D and S effects following the successive duplication events of the D lineage from A and B lineages, scenario #3 referenced as

−

(i.e. with S for short arm, L for long arm and C for centromeric region) ‘(B A) → D’.

[30].

Recently, a third scenario have been proposed suggesting that 4. Translational research in Triticeae

the gene content of A and B subgenomes is more similar to D

than to each other at the whole chromosome level and at the Paleogenomic data and derived modern karyotype orga-

gene sequence relatedness [15,31]. Based on 275 reconstructed nizations, illustrated as a mosaic of reconstructed ancestral

gene trees between hexaploid and diploid wheat species, show- protochromosome (either AGK or ATK segments, Fig. 1), allowed

ing that A and B subgenomes are more similar to the D individually the presentation of modern Triticeae chromosomes as crop circles

than they are to each other, the authors proposed that the bread [32] as reﬁnement of the model initially proposed in the 90s for

wheat genome has been shaped through two rounds of hybridiza- the grasses by Mike Gale’s group [33]. Fig. 3 (top) shows the ‘Trit-

tion between A and B genomes, giving rise to the D genome [31]. iceae syntenome circles’ involving three Triticeae species of major

In this scenario the hybrid origin of the D lineage deriving from an agronomic interest, wheat–barley–rye. For any radius of the circles

equal contribution of the A and B lineages may explain the reported a 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 7

protochromosomes (color code, right), with barley (inner circle referenced as ‘Hv’ circle for Hordeum vulgare) as its modern representative. The external concentric circles

illustrate 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 Triticum

aestivum subgenomes A, B and D) based on the sequenced/mapped gene orthologs (colored vertical bars on the circles). BOTTOM – Screen capture of the PlantSyntenyViewer

web tool [http://urgi.versailles.inra.fr/synteny-wheat] visualizing the synteny between ATK, Brachypodium, rice, maize, sorghum and providing the COS gene information

(ID, primer pairs, SNP in wheat). (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of the article.)

marker development, (ii) improving conserved gene annotation or resolution of synteny-based COS markers has been used in wheat (i)

(iii) candidate gene selection for traits of interest (either conserved to reﬁne metaQTL intervals and immediately beneﬁt from the COS

or lineage-speciﬁc ones) [34]. markers to access robust links with sequence genomes and precise

Such high resolution and large-scale comparative genomics orthologous candidate genes as illustrated for nitrogen use efﬁ-

information offer a tremendous set of gene-based markers that ciency [36], grain ﬁber content [37], carotenoid content [38] traits,

can be used directly as founder resource for genome mapping and and (ii) as a matrix for physical map construction [39].

ultimately trait dissection. Regarding the synteny-based selection Overall, the Triticeae syntenome and more generally the grass

of genic markers, the robust identiﬁcation of collinear regions (i.e. syntenome, delivered through a public web interface PlantSyn-

radius of the syntenome circles) delivered 16464 COS (conserved tenyViewer at http://urgi.versailles.inra.fr/synteny-wheat, can be

orthologous set) markers for SNP discovery in grasses [30,35]. Such considered as a guide for accelerated dissection of major

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

agronomical traits in wheat [30,34]. Fig. 3 illustrates the PlantSyn- [17] M.C. Luo, Y.Q. Gu, F.M. You, et al., A 4-gigabase physical map unlocks the

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Besides, structural comparisons of the grasses and more

diversity using a high-density 90 000 single nucleotide polymorphism array,

particularly the Triticeae genomes, integration of NGS-based

Plant Biotechnol. J. 12 (2014) 787–796.

transcriptome and methylome data in the provided Triticeae syn- [20] J. Ren, D. Sun, L. Chen, et al., Genetic diversity revealed by single nucleotide

polymorphism markers in a worldwide germplasm collection of durum wheat,

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