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Review

The Exceptionally Large Genomes of the Fabeae Tribe: Comparative Genomics and Applications in Abiotic and Biotic Stress Studies

by
Carmen Santos
*,† and
Susana Trindade Leitão
†
Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Av. da República, 2780-157 Oeiras, Portugal
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2024, 14(1), 77; https://doi.org/10.3390/agriculture14010077
Submission received: 15 November 2023 / Revised: 22 December 2023 / Accepted: 28 December 2023 / Published: 30 December 2023
(This article belongs to the Special Issue Genomic Approaches to Understand Crop Response to Biotic and Abiotic Stress)
Versions Notes

Abstract

:
The Fabeae tribe comprises five legume genera, which include some of the most ancient and important crops, like peas, lentils, and faba beans. Biotic and environmental stresses are major threats to the stable and high productivity of Fabeae crops. The use of omics resources can provide breeders with the tools needed to develop new crop varieties in a more efficient and sustainable way. However, the genomic efforts on Fabeae crops have lagged behind compared to other legume species, mainly due to their large genome size and repeat content. The first annotated chromosome-level reference genome assembly in Fabeae was published for pea (Pisum sativum cv. Caméor) in 2019. Since then, many efforts have been made to sequence the genome of other species from this tribe. Currently, 17 genomes of Fabeae species are available for the scientific community; five of them are at the chromosome level. Fundamental knowledge and molecular tools for breeding have been boosted on the legume resistance/tolerance against biotic and abiotic stresses by the availability of some of these recent reference genomes, especially the pea cv. Caméor genome. This review provides a comparison of the Fabeae tribe genomes available and an overview of recent accomplishments in their application in abiotic and biotic stress research.

1. Introduction

The legume family (Fabaceae) includes some of the most important crops for human and animal nutrition worldwide and contributes to environmentally friendly agriculture due to the symbiotic natural ability to fix atmospheric nitrogen. The current focus in legume research is on accelerating genetic gains related to yield, nutritional quality, and stress resistance/tolerance [1].
Legume cultivation is affected by lower crop yields due to biotic and abiotic stress factors [2,3]. Plant response to these stresses is known to involve several genes [4]. Genome sequencing allows for the decoding and understanding of the mechanism or genetic basis for the functional characterization of genes that have a great impact on crop improvement. The development of next-generation sequencing (NGS) technologies and bioinformatics brings the possibility of sequencing any genome or transcriptome [5]. Among legumes, the genome sequence of the soybean (Glycine max) was the first to be completed in 2010 [6]. Other model, crop, and orphan legume species have the whole-genome sequences available since the last decade, including barrel medic (Medicago truncatula) [7], common bean (Phaseolus vulgaris) [8], mung bean (Vigna radiata) [9], and pigeonpea (Cajanus cajan) [10]. Only recently, larger-sized genomes of important crop legumes such as faba bean (Vicia faba) [11], pea (Pisum sativum) [12,13,14], and lentils (Lens culinaris) [15] have been reported.
The availability of genome sequences and large-scale genomic resources facilitates the advances in functional genomics and molecular breeding, which have enhanced the efficiency and resolution of genetic mapping, marker-trait association, and genome-editing studies in legume research [16,17,18,19,20]. Nevertheless, genome assemblies developed for several legume crops are based on short reads (Illumina sequencing-based), have uneven sequencing depths and are fragmented [21]. Whole-genome duplication (WGD) events and extensive repeat content are the main challenges for assembling legume plant genomes.
The majority of legume genome crop genome sizes range from 0.3 to 1.5 Gbp [22]. In the Fabaceae family, the tribe Fabeae presents the largest amounts of DNA within a haploid chromosome set C-values, varying between 1.8 to 13 Gbp [11], exceptionally larger genomes compared to the closely related Trifolieae (genome size ~1.05 Gb) and Cicereae (genome size ~1.27 Gb) [23]. This variation in size and expansion/contraction has occurred during its evolution due to the presence of repetitive DNA. The tribe Fabeae comprises five genera (Lathyrus L., Lens Mill., Vicia L., Pisum L., and Vavilovia Fed.) and includes several important crops, such as peas, lentils, and faba beans [24]. In addition to crops of worldwide importance, the tribe also contains minor crop species (e.g., Lathyrus sativus L.), forage or green manure species (e.g., Vicia sativa L. and V. villosa L.), and ornamental species (e.g., L. odoratus L. and L. tuberosus). Despite the importance of this group, only recently, the genome sequence of some species began to emerge and became available to the scientific community: Pisum sativum [12,13,14], Lathyrus sativus [25,26], Lathyrus tuberosus [27], Vicia sativa [28,29,30], Vicia faba [11], Lens culinaris and Lens ervoides [15]. This review aims to compare the genomes available from the Fabae tribe and explore their application in abiotic and biotic stress studies.

2. Fabeae Tribe Genomes

2.1. Pisum sativum

Pea, commonly known as dry, green, or field pea, is the second most important grain legume in the world after the common bean, being a valuable source of dietary proteins, mineral nutrients, complex starch, and fibers with proven health benefits [31]. Pea was the original model organism used in Mendel’s discovery of the inheritance laws, making it the foundation of modern plant genetics [32]. After Mendel studies, subsequent pea genomics was neglected compared with other plant species. Recently, in 2019, the genome of Pisum sativum cv. Caméor was published as the first annotated chromosome-level reference genome assembly in the tribe Fabeae [13]. Since then, many efforts have been made to sequence the genome of other species in this tribe.
Regarding the Pisum genus, the National Center for Biotechnology Information (NCBI) repository reports six genomes, all for P. sativum (Table 1): two genomes at the chromosome level [12,13], two genomes at the scaffold level (unpublished) and two at the contig level [14,33]. The two chromosome-level reference genome assemblies include the “Pisum_sativum_v1a”, of a French pea cultivar “Caméor” [13], and the more recent reference genome for pea “CAAS_Psat_ZW6_1.0” of the Chinese pea variety Zhongwan 6 (ZW6) [12]. The other pea contig level genome assemblies comprise the “PSA_r1.0” of the pea cultivar JI128, provided by John Innes Centre, UK [14], the “ASM301357v1” of a pea cultivar “Gradus No 2” from the Earlham Institute UK, and the “ASM2453087v1” of a Russian pea cultivar “Frisson” (Table 1). The NCBI repository also includes the Pisum sativum CEN6 assembly (GenBank GCA_947076115.1), but this assembly only covered a 177.6 Mbp region of pea chromosome 6 and not the complete genome [33].
Pisum sativum (2n = 2x = 14) has a large and complex genome, with an estimated size ranging between 3.7 and 4.5 Gbp, containing about 85% repetitive DNA. Sequencing coverage in pea genomes has varied from 44 (cv. JI128) to 281-fold (cv. Caméor) (Table 1). To overcome the challenges of size and repetitiveness, a combination of long-read sequencing developed by Pacific Biosciences or Oxford Nanopore with Illumina short-read DNA data has been useful for genome assembly [12,13,34]. Since long-read sequencing has a higher error rate than short-read Illumina or Ion sequencing, hybrid sequencing or increasing coverage can greatly improve the accuracy of genome assembly.
Assembly complementary approaches have been combined to obtain the pea reference genomes, including high-throughput assembly analyses and manual curation steps [12,13]. In the pea cv. Caméor genome, Illumina short-read sequences were assembled into contigs and then combined into scaffolds using long-range PacBio RSII (Pacific Biosciences) sequences and whole-genome profiling of a bacterial artificial chromosome (BAC) library. Scaffolds were manually curated for inter and intrachromosomal chimeras using sequences obtained from single chromosomes isolated by flow cytometry and an ultra-high-density skim genetic map obtained by genotyping-by-sequencing. Curated scaffolds were then integrated into super-scaffolds using BioNano(San Diego, Califórnia, EUA) genomic maps (optical maps from BioNano Genomics). Finally, the seven pseudomolecules representing the seven pea chromosomes were obtained by anchoring super-scaffolds onto high-density genetic maps [13].
For the pea cv. ZW6 genome, a novel assembly was generated based on the PacBio SMRT long-read sequencing, combining 10x Genomics scaffolding, BioNano optical mapping, chromosome conformation capture (Hi-C) scaffolding, and Illumina technologies [12]. The initial assembly was polished by iterative scaffolding and manual curation, and the final assembly was anchored into seven chromosome-level pseudomolecules, two organelle genomes, and 1572 unplaced contigs. The pea cv. ZW6 assembly strategy resulted in an improved reference genome in continuity and quality of complex repeat regions and transposable elements that remained as gaps in the pea cv. Caméor genome [12,13]. The total size of anchored contigs was 3719.6 Mb, constituting 97.96% of the pea cv. ZW6 genome, whereas anchored contigs constituted only 82.51% of the pea cv. Caméor assembly. The cumulative length of unknown sequences was 10.3 Mb for pea cv. ZW6, which was smaller than the 760.8 Mb observed in pea cv. Caméor.
Less complex assembly methods were applied for the genome assembly of pea cv. JI128, where only the long reads were used. Sequencing errors in the assembly were then corrected, for which Illumina and MGI short reads were employed. Assembly was then anchored to the reference genome of cv. Caméor and Gradus No2 assembly using SNPs obtained by ddRAD (double-digest restriction site-associated DNA)-Seq, as anchors. Information about the methodology for genome assembly of the Gradus No2 and Frisson is not available yet (unpublished studies).
Annotation of pea genomes has been focused on the identification of repetitive elements and prediction of coding genes. The total length of repetitive elements in pea cv. ZW6 was 3249.5 Mbp, larger than in pea cv. JI128 (2825 Mbp) and in pea cv. Caméor (2662.5 Mbp). The majority of the repetitive elements found in these genomes corresponded to transposable elements (TE), from which the long terminal repeats (LTR) retrotransposons were the most abundant in the three annotated pea genomes. In particular, Ogre elements are a type of Ty3/Gypsy LTR retrotransposon first discovered in legumes [35,36] characterized by their large size (reaching 25 kbp) and the presence of an additional ORF (open reading frame) encoding a protein of unknown function located upstream of the gag gene, usually present in LTR retrotransposons [37]. In the Fabeae tribe, Ogre elements typically make up about 40% of the entire genome (22.5–64.7%), and they are considered the major force driving the evolution of the genome size in this tribe [38]. This high level of repetition emphasizes the difficulty of assembling the genomes of Fabeae members and the need for long sequence reads that can span repetitive regions. In pea cv. Caméor, LTRs represented 72.7% of the genome (1,707,747 copies), with Ogre elements being the major representative [13].
The pea cv. ZW6 genome showed a much higher number of full-length LTR (62,978) than pea cv. Caméor (9999) and a higher percentage of active and longer LTRs [12]. The difference in the number of these repetitive elements identified in both pea genomes may justify the differences in genome assembly gap size between the pea cv. ZW6 6 (10.3 Mbp) and pea cv. Caméor (760.8 Mbp). Indeed, the LTR assembly index (LAI), which evaluates assembly continuity, indicated a substantial improvement in LTR completeness for pea cv.ZW6 (LAI  =  13.31) compared to pea cv. Caméor (LAI  =  2.09). In pea cv. JI128 assembly, LTRs occupied about 69% (2284 Mbp) of the genome assembly [14].
Pea protein-coding genes have been annotated using a combination of ab initio, homology-based, and transcriptome-based prediction. In the pea cv. In the JI128 genome, 531,242 potential protein-coding genes were predicted, and the pea genome had more predicted genes [14]. Similar numbers of predicted coding genes were reported for pea cv. Caméor (44,756 complete and 29 truncated genes) and pea cv. ZW6 (47,526). Also, similar average gene lengths were obtained between these two pea genomes: 124.6 Mbp for pea cv. Caméor, and 121.84 Mbp for pea cv. ZW6, respectively.
Pea genome assemblies and gene set completeness have been assessed by Benchmarking Universal Single-Copy Orthologs (BUSCO) using the “embryophyta_odb10” model. Assembly completeness varied from 91.5 (Gradus no. 2) to 99.38% for pea cv. ZW6 (Table 1). The protein mode BUSCO completeness of annotated genes was also higher in pea cv. ZW6 (97.77%) than that in pea cv. Caméor (93.99%) [12].
High-quality reference genomes and annotations provide fundamental resources for functional genomics, characterizing genetic traits, and breeding in crops. The pea cv. Caméor and ZW6 genomes revealed insights into legume genome evolution and domestication and provided important resources for functional genomics and crop breeding [13]. Indeed, the availability of the first pea assembly genome (cv. Caméor) revealed genomic rearrangements across legumes and suggested a major role for repetitive elements in pea genome evolution [13]. Phylogenetics and paleogenomics showed genomic rearrangements across legumes and suggested a major role for repetitive elements in pea genome evolution. Compared to other sequenced legume genomes, the pea genome shows intense gene dynamics, most likely associated with genome size expansion when the Fabeae diverged from its sister tribes [13]. The pea genome is differentiated from its Ancestral Galegoid Karyotype through at least three chromosomal fissions, four fusions, and a translocation between chromosomes Ps1 and Ps5 [13]. Genome expansion in plants is primarily driven by WGD events and the proliferation of TEs. LTRs account for most of the genome size differences between P. sativum and M. truncatula, Trifolium pratense L., L. japonicus, P. vulgaris, or G. max [13].
Besides the pea cv. ZW6 reference genome, Yang et al. [39] also reported a pea pan-genome based on 118 accessions. Pan-genomes comprise the genomic diversity of a species, including core, variable, and unique genes found in a large set of individuals. The whole-genome resequencing and transcriptome data obtained for JI128, JI4, and an F2 population (JI4 × JI128, n = 167) may facilitate pan-genomic future studies in pea [14].

2.2. Lathyrus spp. (L. sativus and L. tuberosus)

After pea cv. Caméor reference genome publication, Emmrich et al. [40] reported a draft genome of a close phylogenetic relative, Lathyrus sativus (grass pea), using a European accession (LS007). Indeed, these authors generated two assemblies of this genome: the EIv1 using short-read Illumina paired-end sequencing and the Rbp combining the Illumina paired-end with long-read Oxford Nanopore Technologies sequencing (PromethION nanopore). More recently, the Rbp genome assembly was also annotated [26]. The Rbp genome assembly and annotation (at scaffold level) is deposited in NCBI as “LS007 EIv1 GenomeAssembly” and deposited on Zenodo [https://zenodo.org/record/7390878], accessed on 15 November 2023. Another grass pea genome assembly became available at the scaffold level, the “ASM2687324v1” of an Indian grass pea cultivar (Pusa-24) [25]. The Pusa-24 L. sativus genome is also available at https://lathyrusgenome.nabi.res.in/index.html online platform, accessed on 15 November 2023, which provides BLAST tools, an ortholog search tool, and direct download of the assembled genome, and associated files. Additionally, an assembly at the contig level is also available for L. tuberosus [27].
Grass pea (2n = 2x = 14) is an important food security crop due to its resilience under hostile environmental conditions, such as drought [41,42]. The crop has a long history in agriculture, but its cultivation has declined, probably due to the presence of the neurotoxin β-ODAP [41,43]. This neurotoxin has been connected with a neurological disease (neurolathyrism) that occurs when grass pea is the main source of nutrition in an unbalanced diet for prolonged periods [44]. The recent available genetic and genomic resources may facilitate breeding for β-ODAP low content. Still, resistance to biotic stress is the main target for breeding in Lathyrus spp. [43,45].
Another Lathyrus species, L. tuberosus (“tuber vetchling”, 2n = 2x = 14), has been cultivated for flavorings, fodder (from leaves), oil (from seeds), and as a potato-like food (from tubers) [46]. To aid future domestication programs for this legume plant and facilitate evolutionary studies of tuber formation, genetic and genomic resources are needed for this tuberous legume [27].
The genome size of Lathyrus species varies from approximately 3.5 to 14.3 Gbp (Lathyrus vestitus), the largest known diploid legume genome [22]. From the genome assemblies available, L. sativus genome size varied from 6.517 ± 0.023 Gbp to 6.620  ±  0.095 Gbp, using the pea genome as standard [25,26]. The length of the EIv1 assembly is 8.12 Gbp, including 1.9 Gbp of Ns in scaffolds [40]. For L. tuberosus, the estimated genome size is 6.8 Gbp [27].
Hybrid assembly methodologies have been used in the L. sativus assembly genomes available, involving short sequencing data (Illumina) with long sequencing data (Pacific Biosciences, Menlo Park, Califórnia, EUA (PacBio) or Oxford Nanopore Technologies, Oxônia, Reino Unido (PromethION)) [25,26,40], while the PacBio was chosen to generate the L. tuberosus draft genome assembly [27]. For Rbp assembly, after filtering for reads >5 kbp and using a long-read assembler, Redbean produced an assembly of 6.2 Gbp based on 34.6X coverage. The resulting assembly contained 162,985 contigs, with a contig N50 of 155.574 kbp and a GC fraction of 38.8%. Following polishing with more assembly algorithms, incorporating 49.7x coverage of paired-end Illumina HiSeq data resulted in an assembly of 6.237 Gbp in 162,994 contigs with an N50 of 157.998 kbp. Hybrid assembly of Pusa-24 was carried out using the default parameters in MaSuRCA [47]. The contig-level assembly covered 3.8 Gbp of the genome with a contig N50 value of 78.27 kbp and a GC fraction of 38.32% (Table 1).
Sequence reads from L. tuberosus were assembled with HIFIASM genome assembler [48], resulting in 1353 contigs with a total length of 6.8 Gbp, a contig N50 of 11.1 Mbp and a GC content of 38.3%, including five mitochondrial and a single chloroplast contigs [27]. Assembly BUSCO analysis showed 96.6% completeness (Fabales). Since L. tuberosus is thought to be an obligate outcrosser, heterozygous regions seem to be present in the assembly, which was indicated by the high degree of BUSCO groups (up to 30%) [27].
Due to the high level of fragmentation, Hi-C scaffolding of L. sativus Rbp assembly only resolved 42.7% of the assembly assigned to 7 chromosome-scale and 2 sub-chromosome-scale scaffolds [26]. The L. sativus cv. The Pusa-24 assembly genome was scaffolded by aligning Pusa-24 contigs to the Pisum sativum cv. Caméor v1a assembly. The scaffolded assembly contained seven chromosome-sized scaffolds and 25,404 contigs. The N50 value of the scaffolded assembly was 421.39 Mbp. This approach results in loss of cv. Pusa-24 genomic regions that were not mapped to the pea genome and may miss chromosomal rearrangements between pea cv. Caméor and grass pea cv. Pusa-24. In particular, it is relevant to clarify if the pea translocation between chromosomes Ps1 and Ps5 compared to the ancestral Galegoid karyotype [13], which is present in Pisum sativum sativum lineage, but not in P. sativum elatius, is also present in grass pea. Given the limitations in both L. sativus (Rbp and Pusa-24) assembly approaches and consequent limitations on annotation procedures, a new L. sativus genome assembly is still needed for future research on this promising species.
Annotation of Lathyrus genomes is only available for L. sativus and includes the identification of repetitive elements and prediction of coding genes. For Rbp genome assembly, annotation, and downstream analysis were conducted with the complete (6.2 Gbp assembly), unscaffolded assembly, aiming to not lose sequences of potentially important genes that were not scaffolded [26]. Gene models were predicted by an evidence-guided annotation approach incorporating RNA-seq of the three grass pea genotypes and cross-species protein alignments. In total, 30,167 high-confidence protein-coding genes and 15,307 low-confidence protein-coding genes were identified. For the Pusa-24 assembly genome, gene models were predicted by combining ab initio gene prediction, homology-based, and RNA-seq data. The final gene set consisted of 50,106 genes. The protein mode BUSCO completeness of annotated genes was higher in L. sativus Pusa-24 (96.0%) than in that Rbp assembly (82.6%), using Fabales as a model. Repetitive sequences represented 80.61% in Rbp assembly and 83.31% in Pusa-24 assembly. LTR elements were the most abundant in both grass pea assemblies, accounting for 78.3% of the contig lengths in Rbp assembly and 37.58% of the whole genome of Pusa-24 [25,26].
Further, to confirm the validity and quality of gene prediction of the Lathyrus sativus assemblies, researchers have searched for genes that contribute to β-ODAP biosynthesis. Since β-ODAP, an endogenous non-protein amino acid, is present exclusively in Lathyrus spp. and not in the other legumes, identification of the biosynthetic genes of this non-protein amino acid in the current genome assemblies further affirms the quality of the gene prediction. Edwards et al. [26] have elucidated the biosynthetic pathway leading to the β-ODAP formation. The final reaction of the pathway depends on an interaction between L. sativus acyl-activating enzyme 3 (AAE3) and a BAHD-acyltransferase (BOS) that forms a metabolon activated by CoA to produce β-L-ODAP. AAE3 participates in oxalate catabolism across various plant species, including M. truncatula. However, in L. sativus, an evolutionary repurposing of this established pathway results in the generation of β-L-ODAP. This alteration potentially offers an alternative method for eliminating oxalate [26]. Rajarammohan et al. [25] have identified the assembly of most of the known genes associated with the β-ODAP biosynthetic pathway in the Pusa-24 genome: viz. Serine O-acetyltransferase (SAT), cysteine synthase (CS), cyanoalanine synthase (CAS), nitrilase, β-ODAP synthetase (BOS), oxalyl-CoA synthetase (OCS), and oxalate decarboxylase (ODC). Despite the assembly limitations discussed above, the results on the prediction of genes from the biosynthesis of β-ODAP are indicative of the high-quality overall completeness of the predicted gene set of the L. sativus genome assemblies and may be used for other gene discovery studies.

2.3. Vicia spp. (V. faba, V. sativa, and V. villosa)

The genus Vicia L. counts 150–210 species distributed across Europe, Asia, and North America, but mainly in the Mediterranean [49]. The best-known species of this genus is the faba bean or broad bean (V. faba, 2n = 2x = 12), an important food legume and fodder crop with nutritional relevance in the human diet. Faba bean is one of the earliest domesticated crops, dating back over 10,000 years in the near East. While no known wild progenitor exists today, it holds promise as a solution to future protein demands due to its high yield and protein content (around 29%), surpassing other cool-season pulses like peas, lentils, and chickpeas [50]. However, the faba bean has posed challenges for breeders because of its partially allogamous mating system, large genome size, and low seed multiplication rate.
Other vetches species, such as common vetch or spring vetch (V. sativa) and hairy vetch (V. villosa), with smaller protein-rich seeds, are normally used for animal feed (forage, fodder, pasture, silage, hay) and as cover crop due to their fast biomass production.
Four Vicia assembled genomes are available for the research community in NCBI: one of V. faba (cv. Hedin/2 genome v1), two of V. sativa (ASM2176476v1, and VSA_r1.0), and one of V. villosa (Vvil1.0). Their sizes range from 1.7 (V. sativa) to 11.9 Gbp (V. faba). Vicia fava Hedin/2 genome v1, V. sativa ASM2176476v1, and V. villosa Vvil1.0 are chromosome-level assemblies and the current reference genomes for the three species (Table 1). The assembly V. sativa VSA_r1.0 is a scaffold-level assembly. VfEP_Reference-Unigene is also listed in NCBI as a V. fava genome; however, it corresponds to a transcriptomic study. The raw sequence reads of V. sativa cv. Lanjian No. 1 is also included in NCBI in the project PRJNA730328. Vicia faba cv. Hedin/2 reference genome v1, the V. sativa ASM2176476v1, VSA_r1.0, and V. villosa Vvil1.0 are annotated. This genotype was chosen as a reference for the genome sequencing due to its high autofertility, productivity, early maturing spring habit, and homozygosity. Despite not being available in NCBI, there is a second faba bean genome assembly using the German variety, Tiffany [11]. The Faba Bean Genome Consortium made available the genome assemblies files and genome browser tools for both cv. Hedin/e and Tiffany at www.fabagenome.dk, accessed on 15 November 2023.
The Faba bean genome is massive, primarily due to the proliferation of repeat elements like retrotransposons and satellite repeats [11]. Despite its enormous size (11.9 Gbp for Hedin/2 and 11.4 Gbp for cv. Tiffany), it is surprisingly compact in terms of gene distribution, with genes and recombination events evenly dispersed across chromosomes. This compactness, however, is influenced by substantial copy number variation driven by tandem duplication. The faba bean genome is also noteworthy for being one of the largest diploid field crops, with its largest chromosome holding the equivalent of an entire human genome. Notably, there is no evidence of recent whole-genome duplication in the faba bean genome [11]. Nevertheless, more genes are duplicated in the faba bean genome compared to peas and lentils. Similar to other Fabeae members, LTR retrotransposons are an extensive part of the genome, almost 80% of the Hedin/2 and Tiffany assemblies [11]. LAI score of 10.5 was calculated for Hedin/2 assembly, providing evidence for its contiguity.
The genome sequence of cv. Hedin/2 was obtained using PacBio HiFi long reads, resulting in 20-fold coverage, N50 of 2700 kbp, a total contig number of 10,721, and 34,221 protein-coding genes (Table 1).
The GC content was 37.3%. The annotation was performed using RNA-seq data from nine tissues. Gene order was highly collinear and syntenic with M. truncatula and P. sativum. The gene model predictions captured 96% of single-copy conserved orthologues according to the BUSCO analysis with the Embryophyta database. To further validate the gene annotation, several M. truncatula genes related to symbiosis with rhizobia or arbuscular mycorrhizal fungi were aligned, and putative orthologues were found for all those genes [11].
A similar number of gene models was also predicted in the assembly of cv. Tiffany using HiFi data (ten-fold coverage, N50 of 1600 kbp, a total contig number of 14,378, and 34,043 protein-coding genes, Table 1) [11]. Genetic mapping and Hi-C data were used to place a large portion of the genome (94%) into chromosomal pseudomolecules, providing a valuable frame of reference for genetic mapping, gene expression profiling, and comparative genomics. A higher proportion of BUSCO duplicate genes was obtained in Tiffany than in Hedin/2, leading to the need for the removal of ~10% of short-contig sequences in Tiffany to reach a similar low gene duplication level as in Hedin/2 (0.37%). For the Hedin/2 annotation, 69% of gene models were supported by RNA-seq data. In addition, 93.3% and 93% of gene models for Hedin/2 and Tiffany had similarities to proteins of close relatives (pea, lentil, Medicago, e-value cutoff 1 × 10−5). Close to 80% of the Hedin/2 assembly was annotated as transposon-derived. Most of them (63.7%) are LTRs. Indeed, around 44% of the genome is made of Gypsy elements from the Ogre LTR retrotransposons family. The fact that the length of each Ogre element is up to 35 kbp partially explains the giant size of the faba bean genome [11].
Regarding V. sativa, three high-quality chromosome-level reference genomes were recently assembled using the cultivars Studenica, KSR5, and Lanjian No. 1 [28,29,30]. For this species, at least three different chromosome numbers (2n  =  10, 12, and 14) are described, making 2n = 12 the best-characterized karyotype [29]. For Studenica V. sativa, Xi and colleagues [30] used a combination of long-read Oxford Nanopore sequencing, short-read Illumina sequencing, and high-throughput chromosome conformation data (CHiCAGO and Hi-C) analysis. The sequencing was performed on a PromethION and Novo-Seq 6000 (Illumina NovaSeq 6000 Sequencing System). GenomeScope analysis estimated a genome-wide heterozygosity level of 0.09% and a genome size of 1.61 Gbp, slightly smaller than the flow cytometry estimate of 1.77 Gbp. The final genome assembly comprises six pseudo-chromosomes, with 1.65 Gbp of contigs anchored to them, leaving 10 contigs (overall 334,511 bp length) unassigned. The overall genome size was calculated as 1.653 Gbp, with a GC content of 35.6% (Table 1). The BUSCO analysis indicated a genome completeness of 98% of the dicotyledonous orthologs, with 9% representing duplicated genes. A total of 9990 assembled contigs were obtained with an N50 value of 685 kbp. RNA-seq analysis and gene modeling enabled the annotation of 53,218 protein-coding genes. BUSCO analysis identified 95.6% (Fabales) of completeness. The LTR elements constitute 64.2% (22.5% are Ogre elements) of this genome [30]. The high value of LAI (12.96) calculated suggests a reference quality of the Studenica V. sativa genome. Another draft genome sequence (VSA_r1.0) for common vetch was developed by Shirasawa et al. [29] using the Japanese standard inbred line KSR5, HiSeq2000 (Illumina), and RSII (PacBio) instruments. The genome size was estimated to be 1.769 Gbp, and the assembly size was 1.541 Gbp. The total number of scaffolds was 54,083, and the N50 was 90.1 kbp. Around 50% of the genome length is constituted by repeat sequences, 13% of which are assigned as LTR elements. According to BUSCO analysis, 77.5% of the genome was completely assembled, and the ortholog completion was 94.1%. In addition, Ma and colleagues [51] carried out a genome survey sequencing of common vetch on the Chinese cultivar Lanjian No. 1. The Illumina NovaSeq 6000 instrument with PE 150 sequencing methods was used to construct and sequence a genomic paired-end library with 300–400 bp short-inserts. A total of 79.84 Gbp of high-quality sequence data were obtained and assembled into 3,754,145 scaffolds, with an N50 length of 3556 bp. The K-mer analyses estimated the genome size to be 1.57 Gbp, the heterozygosity rate to be 0.4345, and the GC content to be 35% (Table 1). These results are very close to the ones obtained for the Studenica cultivar [28]. The assembled scaffolds were employed for genomic microsatellite (SSR) search, and 76,810 putative SSRs were identified.
Recently, Fuller et al. [52] disclosed a high-quality reference genome assembly for hairy vetch, V. villosa, using the cultivar AU Merit. They chose this cultivar because it can be clonally propagated in tissue culture. The genomic short-read libraries were sequenced on an Illumina NextSeq 500 instrument. The GenomeScope tool estimated the haploid genome size to be 0.883 Gbp, with an elevated heterozygosity of 3.14%, likely a result of the cross-fertilizing nature of V. villosa. Hi-C genome scaffolding was employed to create chromosome-scale scaffolds. The resulting Vvill1.0 assembly consisted of 1888 scaffolds totaling 2,034,988,938 bp, substantially larger than the GenomeScope haploid genome size estimate but in line with previous estimates of 2.04 Gbp [38]. The assembly had a scaffold N50 of 174.24 Mbp and a GC content of 35.62% [52] (Table 1).
Seven scaffolds in Vvill1.0 represented haploid representations of the seven estimated linkage groups for V. villosa, accounting for 67.74% of the total genome assembly size [52]. Roughly one-third of the assembly was impossible to assign to linkage group scaffolds due to the high heterozygosity of the sequenced individual. This high heterozygosity is probably due to the cross-pollinating nature of V. villosa in comparison to the more selfing nature of V. sativa. A total of 5373 contigs were obtained with an N50 of approximately 600 kbp (Table 1). The repetitive content in Vvill1.0 was similar to that of the V. sativa reference assembly, with 81.1% of the assembly consisting of identified repeats, compared to 83.9% in V. sativa. Vvill1.0 was predicted to have an LAI of 22.5, categorizing it as a high-quality reference genome in the “gold” category due to the assembly fidelity of repeat elements. Using prediction and RNA-seq evidence, the authors identified 53,321 protein-coding genes, with 81.8% of them annotated [52].

2.4. Lens culinaris and L. ervoides

Lentil (Lens culinaris Medik.) is a self-pollinated legume crop with a diploid chromosome number of 2n = 2x = 14. Originating from the Middle East and Central Asia, lentil is now cultivated worldwide and serves as an important source of plant-based protein [53]. It is a dietary staple in many Middle Eastern and South Asian countries and is gaining popularity in other regions due to its cooking flexibility and suitability for diabetic, gluten-free, and heart-smart diets [15].
To improve lentil’s important traits like disease resistance, environmental stress tolerance, and agronomic and quality traits, efforts have been made to introduce novel alleles from the wild gene pool into elite cultivated backgrounds. Lens ervoides (Bring.) Grande was initially used as a source of disease resistance, and it also offers variability for seed quality and yield traits [54,55].
In a recent study, Ramsay et al. [15] assembled the genomes of two lentil species: the Canadian red L. culinaris cultivar CDC Redberry and the wild L. ervoides accession IG 72815. The L. culinaris reference genome (Lcu.2RBY; CDC Redberry) was assembled using 54x long-reads, polished with both Oxford Nanopore long reads and additional Illumina short reads. Hi-C proximity and a single genetic map were used to scaffold contigs into seven pseudomolecules, covering 92.8% of the 3.92 Gbp estimated genome size (Table 1).
The L. ervoides reference genome (Ler.1DRT; IG 72815) was assembled from 52x long reads, polished with long reads and additional short reads, and similarly scaffolded into seven pseudomolecules, representing 96.1% of the assembly. This assembly is smaller, approximately 2.9 Gbp [15] (Table 1).
Both genomes have a similar number of high-confidence genes, with 39,778 in Lcu.2RBY and 37,045 in Ler.1DRT, representing, respectively, 94% and 95% complete BUSCO with the Fabales database (Table 1). Repeats constitute a significant portion of the CDC Redberry genome, accounting for 82.6% (3.2 Gbp) of the 3.9 Gbp assembly. In IG 72815, the proportion of repeats is lower at 78.3%, with 947 Mbp fewer LTRs, contributing to the smaller genome size. Like the other species from the Fabeae tribe, the repetitive regions primarily consist mostly of LTRs of the Ty3/gypsy type. RNA-seq data from seven tissue samples: flowers, leaflets, seedling roots, root nodules, seedlings, etiolated seedlings, and flower buds was used to assist with the annotation of protein-coding genes in L. culinaris. For L. ervoides, RNA-seq data from Ascochyta lentis-inoculated samples were used for annotation [15].
This study also found high collinearity among pea, Medicago, and the two lentil species, with some notable translocations and inversions. A large, inverted, reciprocal translocation exists between chromosomes 2 and 3 in both Lens species relative to pea chromosomes 1 and 5, suggesting this is a specific feature of the pea genome [15]. Chromosome-level structural variations, such as translocations and inversions, are considered drivers of genome evolution and speciation [56]. Comparative mapping indicated several rearrangements occurred after Lens species diverged from peas and other cool-season legumes but before L. culinaris and L. ervoides diverged [15].
Having genome assemblies for both wild and cultivated lines will facilitate more precise and cost-effective access to the genetic variability available in wild relatives. Mapping sequencing reads to their own genome instead of relying on alignment to a related domesticated species, resulting in more markers, improved QTL analyses, and a better chance of identifying candidate genes [57]. These findings will significantly aid in further research and genetic improvement of lentil as an important crop.

3. Applications in Abiotic and Biotic Studies

With the advances in sequencing and the availability of all these legume reference genomes, SNP discovery and QTL mapping can be performed, and QTLs can be more precisely localized on the genetic and physical sequence maps. This enables a better knowledge of the genetic basis of traits that are important to breeders, facilitating the generation of improved varieties. Nowadays, resistance or tolerance to biotic and abiotic stresses are among the most pressing traits to breed for. With accelerating climate change, increased abiotic stresses are expected to challenge agriculture and food security [58]. High-temperature spikes during crop growth, especially for the most critical reproductive period, are expected to exceed the range encountered during crop domestication [59]. Likewise, biotic stresses, such as pathogen infection and pest infestation, are also affected by changes in temperature and humidity. Warmer and more humid conditions tend to accelerate the development of pests, enabling their range expansion. Consequently, new pathogens and pests could emerge in areas where they have not previously occurred, affecting crops [60]. A summary of applications in biotic and abiotic stress studies using the genomic information from the Fabeae tribe is presented in Table 2.
Pea crop suffers from various biotic stresses, including bacterial, fungal, viral, pest, and nematode infestations, as well as weeds. Among them, fungal diseases are considered to be the major type of biotic stress [2]. After the publication of the first pea genome [13], several studies on legume biotic stresses have been favored by the availability of a pea reference genome. Genetic and genomic studies on legume fungal diseases have been performed in aerial fungal diseases, such as powdery mildew [61,62,63], white mold [69], rust [71,72], ascochyta blight [93,94], and also in root diseases, like fusarium wilt and root rot [76,77,95] and Aphanomyces root rot (caused by oomycetes) [79,80,81]. In these studies, the Caméor pea genome was used for SNP calling, location of SNP physical positions, identification of candidate genes underlying QTLs, and syntenic studies aiming at genetic linkage maps validation and location of ortholog genes of interest by comparative mapping.
Comparative mapping between L. sativus and L. cicera genetic linkage maps and P. sativum cv. Caméor, L. culinaris Medik., and M. truncatula Gaertn. reference genomes revealed important aspects of the conservation of the MLO1 powdery mildew susceptibility gene position and of the overall chromosomal rearrangements occurring during legume evolution [61]. In this study, high synteny between grass pea recombinant inbred line high-density linkage map and the pea genomes was observed. Since the L. sativus genome was not fully assembled before 2023, comparative mapping between Lathyrus species and pea cv. Caméor genome [13] was also used for GWAS, in which SNP markers’ physical positions were assigned based on the pea genome [61,63]. Furthermore, candidate genes underlying molecular markers identified by GWAS and QTL linkage mapping related to powdery mildew, rust, and Fusarium wilt resistance in Lathyrus spp. were predicted by comparative mapping using pea cv. Caméor genome [61,62,63,71,72,76]. Therefore, the availability of the pea genome allows the implementation of more accurate comparative genomics, reinforcing breeding programs through faster and more efficient identification of QTLs and candidate genes. Accordingly, SNP quality assessment and QTL location for partial resistance to Aphanomyces root rot were performed by alignments to the genome. Molecular markers identified as associated with pea resistance; for example, Sclerotinia sclerotiorum and P. pinodes were aligned to the pea genome for candidate gene discovery [69].
Proteomic studies also used pea cv. Caméor genome for identification of proteases secreted by the root pathogen Aphanomyces euteiches during pea infection, using comparison of MS/MS spectral against the reference genome [80,96].
Other studies on biotic stresses have been taking advantage of the Caméor pea genome availability, such as studies on resistance against insects [82,83], the parasitic plant Orobanche crenata [20], herbivores [84], and bacterial blight [97]. In these studies, the pea genome was useful for genotyping using the genome as a reference in GWAS for pea resistance to aphids [82]; comparative mapping between a high-density genetic map and the pea genome for genetic dissection of pea resistance to broomrape (Orobanche crenata) [20]; identification of candidate genes related to pea response to bruchid and herbivores [83,84]; and prediction of grain yield for field pea using bacterial blight disease scores [97]. The ZW6 pea genome was used in a comprehensive dataset of full- and partial-length NLR (nucleotide-binding leucine-rich repeat immune receptors) resistance genes across 100 chromosome-level plant genomes [98]. Plant NLR proteins directly or indirectly detect pathogen effectors activating the effector-triggered immunity (ETI), a robust layer of plant defense against pathogens [99].
Peas are also highly susceptible to abiotic stresses such as drought, heat, and cold conditions. Globally, drought and heat stresses are the most critical pea abiotic stresses, mainly during the flowering stage, while frost, salinity, and early-season flooding diversely affect the growth and yield of the crop. Fundamental knowledge and molecular tools for breeding have been boosted on the legume tolerance against abiotic stresses after peas entered the genomic era with the pea Caméor genome sequenced. Diverse studies have been performed to better understand the legume tolerance mainly to drought [64,65,66,67,68] and heat [19,68,70] stresses but also to frost [73,74], cold [75], and salinity [78]. For drought, the pea cv. Caméor genome has been used for genotyping and GWAS, for example, in the identification of invertases in seeds subjected to drought and protein identification in root nodules under drought conditions [64]. For heat stress, researchers have been using pea cv. Caméor genome for GWAS and further identification of candidate genes for heat adaptative traits [68] and mapping of transcriptomic reads related to the negative effects of heat stress on reproductive growth [70,75]. Similar approaches have been applied to study pea tolerance to frost, including the identification of candidate genes for this trait [73]. Syntenic studies were also performed between QTLs identified in faba bean for frost tolerance and the pea cv. Caméor genome and conservation of genetics for this trait were observed [74]. Mapping of transcriptome and miRNA sequencing reads against pea cv. Caméor genome revealed a microRNA regulation network involved in pea response to cold [75]. Finally, one study on pea photosynthetic performance under salinity conditions used pea cv. Caméor genome for mining ortholog genes and miRNAs of interest in A. thaliana [78].
The other pea assembly genomes available (at scaffold and contig levels) were not used for studies on biotic and abiotic stresses.
Regarding the Lathyrus genome assemblies, no reports on biotic or abiotic studies have been published so far. Nevertheless, the L. sativus Rbp assembly was used to study the macroevolution of NLR genes in legumes, including L. sativus [100]. Studies using L. sativus genome assemblies are focused on the biosynthetic pathways of B-ODAP. Nevertheless, due to the known enhanced resistance and tolerance of L. sativus against biotic and environmental conditions compared to other members of the Fabeae tribe, a reliable and accurate genome assembly will be crucial to understanding the L. sativus mechanisms underlying its response to stresses. Moreover, the development of new precision breeding screening tools will enable more competitive stress-resistant/tolerant Lathyrus and other legume varieties to be selected with increased speed and efficiency, accelerating their future introduction in the market.
The availability of the faba bean genome sequencing will greatly benefit breeders and geneticists, helping them improve sustainable protein production in the Mediterranean, subtropical, and northern temperate zones. It is known that faba bean production is severely affected by drought and cold [51,101,102], foliar diseases such as chocolate spot, Ascochyta blight, and Cercospora leaf spot, insects’ pests such as broad-bean beetles (Bruchus rufimanus) and aphids (Megoura crassicauda, Aphis fabae Scop.), viral diseases including broad bean mottle virus (BBMV), broad bean stain virus (BBSV), bean leaf roll virus (BLRV), and bean yellow mosaic virus (BYMV) [103] and root-parasitic plants, such as broomrape (Orobanche crenata) [104]. Since the publication of V. faba genome assembly is still very recent, few reports on biotic and abiotic stresses have been published using the faba bean genome. The exceptions are three faba bean drought response studies [85,86]. The first study revealed that VfbZIP5 enhanced drought tolerance by reducing the levels of proline (PRO), malondialdehyde (MDA), and peroxidase (POD) [85]. In the second study, it was shown that the expression of VfNR1 is a consequence of hypoxia in the root nodules that occurs in the presence of drought and salt stress [86]. The third is a genome-wide association study (GWAS), in which the faba bean genome, together with the M. truncatula genome, were used to annotate the potential candidate genes identified associated with seed weight, SPAD, and proline content under drought stress [87]. Simultaneously, traits related to seed quality and consumer preferences, such as low alkaloid glycosides vicine and convicine and low tannin content, are expected to be more efficiently targeted for faba bean breeding [105,106]. We foresee, in the near future, the publication of genome-wide association studies aiming at the identification of novel genetic variants and candidate genes controlling the above-mentioned important traits. As a practical application of the genome sequence, the genetic basis of seed size and hilum color was already dissected using high-resolution GWAS, highlighting the role of Vfaba.Hedin2.R1.4g051440 gene in regulating seed size and polyphenol oxidase (PPO) in hilum color variation [11]. Additionally, the introduction of favorable alleles or the genomic edition of elite cultivars to speed up faba bean breeding and obtain new varieties with desirable qualities might be a reality soon. The release of the genome sequence also enables population-scale resequencing of genebank collections, elite cultivars, and mutants, further enhancing research and progress in this vital crop [106].
Moreover, the crucial insights into the genome characteristics of common vetch and hairy vetch offer valuable information to design whole genome sequencing strategies for crop improvement in the future. The availability of chromosome-scale genome assembly for both V. sativa and V. villosa is a significant development for genetic improvement programs targeting these crucial cover crops and forage species. The genomic information available can now assist the breeding for drought and cold tolerance [107,108], and lower content of γ-glutamyl-β-cyano-alanine (GBCA) toxin in common vetch [109], and for Ramularia sphaeroidea Sacc. and Ascochyta viciae resistance [110] and cold tolerance [111] in V. villosa. Additionally, since these species share conserved gene orthologs, they are valuable resources for comparative studies of leguminous plant genomes.
In lentil, the use of a draft version of the L. culinaris reference genome was already useful to improve the quality of an RNA-seq analysis of a defense transcriptome activated by A. lentis infection, in comparison to the de novo assembly of the transcriptome [88]. Also, recent genome-wide association studies benefited from the disclosure of the lentil genome, allowing the unveiling of potential candidate genes in salt tolerance mechanisms, the identification of anthracnose race 1 and stemphylium blight resistance loci, and lentil MLO genes [89,90,91,92].
To our knowledge, there is no report on the use of L. ervoides genome sequence in abiotic or biotic studies. However, this wild relative of lentil has shown tolerance against drought and cold stresses [112] and resistance to key biotic stresses, such as rust (Uromyces fabae (Grev.) Fuckel), fusarium wilt (Fusarium oxysporum f. sp. lentis (Vasd. Srin.) Gord), and powdery mildew (Erysiphe trifolii) [113]. While crossing between these two species is possible, L. ervoides is an accessible and promising source of useful genes/alleles for gene introgression aiming at widening the genetic base of lentils through interspecies crossing [15].
Transposons mediated unequal recombination, which potentially gives rise to the gain or loss of genes in legumes, especially in Fabeae, due to the high number of repetitive elements in this tribe [114]. Differential expansion and removal of these elements probably shaped genomes throughout the evolution of the Fabeae and notably within Pisum, highlighting the repetitive elements as a major driver in the evolution of these large genomes. Additionally, WGD also plays a significant role in plant genome evolution by providing raw materials that can be modified by natural or artificial selection.
Despite Fabeae members having a large size genome, some species reveal an overall contraction of the NLRome, which includes genes involved in plant defense mechanisms [100]. P. sativum and L. sativus have shown the lowest NLR density concerning their genome size. Contrary to this contraction trend, the legume tribe Trifolieae has shown large-scale expansion of NLRome irrespective of their genome size. These data suggest that the expansion and contraction of NLRs are not dependent on genome size [100].
Now that more genomic tools are available, we foresee an increase in the development of functional markers to assist crop breeding by marker-assisted selection. Several examples of functional markers, including cleaved amplified polymorphic sequence (CAPS), co-dominant, and KASPar markers, have been developed for the selection of er1 powdery mildew (E. pisi) resistance in pea cultivars [115,116,117,118]. In lentils, a genetic linkage map between L. culinaris and L. odemensis was developed based on thousands of functional markers (SNPs) mapped in expressed genes for morphological and agronomical traits and QTLs involved in resistance to Ascochyta [119]. Functional genomics approaches are crucial to introduce QTLs/genes associated with biotic or abiotic traits in desirable cultivars in a more efficient and accurate way. Syntenic regions shared between the genomes of different legume species will facilitate future comparative genomic studies.

4. Conclusions and Future Directions

The sequencing of legume genomes has grown very fast in the last decade, leading to an increase in the quantity and quality of publicly available genomic resources. The more advanced, accurate, and fast sequencing technologies, such as long-read sequencing and new computational tools, combined with the declining sequencing costs, have enabled the assembly of the large and complex genome characteristics of legumes. Complete genome assemblies will increase the knowledge of the evolution of the different species. This will have a tremendous impact on the understanding of the genetics and genomics of important agronomic traits, such as biotic and abiotic stress responses, and support legume breeding.
The proportions of repeats (78–85%) of the Fabeae genome assemblies described in this review are much higher than for other diploid legumes, such as Medicago (20–23%), chickpea (Cicer arietinum L.) (49%), pigeonpea (Cajanus cajan (L.) Huth.) (52%), and common bean (Phaseolus vulgaris L.) (45%). This helps to explain the larger size of these genomes in comparison to other diploid plants, but also the rearrangement observed among some of these species, which promoted genome evolution and speciation.
A challenge for the generation of high-quality genome assemblies is the presence of high levels of heterozygosity, observed, for instance, in predominantly outcrossing species like V. villosa and L. tuberosus. High heterozygosity constitutes an important source of assembly error hindering the generation of high-quality reference genomes. This issue might be overcome by using an approach that includes different strategies, such as using longer reads, the combination of more than one assembly technique, both manual and automated data curation, and using gamete binning, a method that allows the separation of the whole-genome sequencing reads into haplotype-specific reads sets [120,121,122].
The growing affordability of long-read DNA sequencing will soon contribute to the creation of pangenomes, incorporating all the genetic diversity within the species belonging to this tribe. The availability of more reference genomes enhances the quality of comparative genomics studies by improving genome synteny analysis [61,123]. Moreover, there is even potential for a more expansive super-pangenome that encompasses not only the species belonging to the Fabeae tribe but also closely related crops [124]. By comprehending this range of genetic differences, breeders can effectively exploit specific genome regions from distantly related wild species, which confer traits like disease resistance and adaptability to different climates. This valuable resource would shed light on the evolutionary journey of legumes and the genomes of their members.

Author Contributions

All authors contributed to literature revision and writing. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Fundação para a Ciência e Tecnologia (FCT, Portugal) through the R&D Research Unit GREEN-IT—Bioresources for Sustainability (UIDB/04551/2020 DOI 10.54499/UIDB/04551/2020 and UIDP/04551/2020 DOI 10.54499/UIDP/04551/2020) and the LS4FUTURE Associated Laboratory (LA/P/0087/2020). CS and STL were also supported by FCT through the Research Contracts by Stimulus of Scientific Employment, Individual Support 2017 and 2022 programs, references 2017.00198.CEECIND (https://doi.org/10.54499/CEECIND/00198/2017/CP1428/CT0002) and 2022.00163.CEECIND (https://doi.org/10.54499/2022.00163.CEECIND/CP1725/CT0021) respectively.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Summary of characteristics and statistics of the Fabeae genome assemblies. n.a. means not available.
Table 1. Summary of characteristics and statistics of the Fabeae genome assemblies. n.a. means not available.
GenomeOnline Platform or Genome Database%GC ContentBiological SamplesSize Genome (Gbp)PloidyGenomic DNA Sequencing TechnologyGenome Coverage (Fold)Assembled Scaffolds (nr/Length Mbp)Contigs (nr/Length Mbp)N50 Contigs (kbp)Complete BUSCO Assembly (%)Protein-Coding Gene Models (nr/Average Length Kbp)Complete BUSCO Annotation (%)
Pisum sativum Caméorhttps://urgi.versailles.inra.fr/Species/Pisum/Pea-Genome-project, accessed on 15 November 202337.6French pea cultivar Caméor4.452n = 14Illumina and PacBio RSII28124,623/3919.1218,010/3159.5837.93196.7844,756/124.693.99
Pisum sativum ZW6https://www.peagdb.com/index/, accessed on 15 November 2023n.a.Chinese pea cultivar Zhongwan 6 (ZW6)4.282n = 14Illumina HiSeqX Tem, SMRT- PacBio seq, Illumina Nova Seq 600085.21579/3796.72402/3786.4898099.3847,526/121.8497.77
Pisum sativum JI128 PSA_r1.0PRJDB10540 (NCBI), accessed on 15 November 202336.5JI128 (Norwich, United Kingdom)4.52n = 14MinION (Nanopore)44n.a.117,981/297.0451.22295.4531,242n.a.
Pisum sativum GradusPRJNA432052 (NCBI), accessed on 15 November 202337.5SAMN08429545 Gradus No 2 (Earlham Institute, United Kingdom)4.32n = 14Illumina HiSeq865,449,423/n.a.5,465,676/4274.31460.191.5n.a.n.a.
Pisum sativum FrissonPRJNA812957 and PRJNA853105 (NCBI), accessed on 15 November 202338ASM2453087v1 Russian pea cultivar Frisson3.72n = 14Oxford Nanopore MinION; Illumina HiSeq1002254/n.a.2355/n.a.5000n.a.n.a.n.a.
Lathyrus sativus Eiv1PRJEB33571 (NCBI), accessed on 15 November 202338.3European cultivar LS0078.12 (including 1.1 Gbp of Ns)2n = 14Illumina HiSeqn.a.669,893 (>1 kbp)59.72882.8 (Fabales)33,819/1.45479.9 (Fabales)
Lathyrus sativus Rbphttps://zenodo.org/record/7390878, accessed on 15 November 202338.8European cultivar LS0076.522n = 14Oxford Nanopore Technologies long-read45.44162,994 (>1 kbp)157.99889.6 (Fabales)63,92282.6 (Fabales)
Lathyrus sativus Pusa-24https://lathyrusgenome.nabi.res.in/, accessed on 15 November 202338.32Indican cultivar Pusa-246.622n = 15Illumina HiSeq. 2500 platform; PacBio Sequel (I) platformn.a.25,411/380580,744/380078.395.96 (Fabales)50,106n.a.
Lathyrus tuberosusPRJNA810344 (NCBI), accessed on 15 November 202338.3Lathyrus tuberosus NL206.82n = 14PacBio HiFi sequencing30n.a.1353/679111,10096.6 (Fabales)n.a.n.a.
Lens culinaris Lcu.2RBYhttps://knowpulse.usask.ca/genome-assembly/Lcu.2RBY, accessed on 15 November 2023n.a.Canadian red cultivar CDC Redberry3.922n = 14PacBio SMRT + Oxford Nanopore Technology34 + 2037606094130094.439,77894
Lens ervoides Ler.1DRTn.a.n.a.Wild accession IG 728152.92n = 14Oxford Nanopore Technology5228702291470095.137,04595
Vicia fabahttps://projects.au.dk/fabagenome//, accessed on 15 November 2023n.a.Hedin/2132n = 12Hedin/2: PacBio HiFi long reads203986/11,90010,721270096.334,22193.3
Vicia fabahttps://projects.au.dk/fabagenome//, accessed on 15 November 2023n.a.German cultivar Tiffany132n = 12Tiffany: PacBio HiFi reads using KAT (v2.4.2)101971/11,40014,378160091.634,04393
Vicia sativa KSR5
VSA_r1.0		https://plantgarden.jp/ja/list/t3908/genome/t3908.G001, accessed on 15 November 2023n.a.Japanese standard inbred line- KSR51.82n = 14HiSeq2000 Illumina (paired-end) and RSII instrument (PacBio)1056,487,000/250054,083 (>1 kbp)90177.531,14694.1
Vicia sativa Studenica
ASM2176476v1		http://gigadb.org/dataset/view/id/100954/File_page/2, accessed on 15 November 202335.6Australian cultivar Studenica (V. sativa subsp. Sativa)1.65–1.772n = 12PromethION, Illumina NovaSeq 6000 Sequencing System, and Illumina HiSeq X Tem124.3 + 43.71 + 98.18n.a.999065997.853,21895.6
Vicia sativaPRJNA730328 (NCBI), accessed on 15 November 202335.94Chinese cultivar Lanjian No. 11.5682n = 12Illumina NovaSeq 6000 Sequencing System/PE150n.a.3,754,145/1,516,858,1864,227,9421.245n.a.n.a.n.a.
Vicia villosa
Vvill1.0		PRJNA868110
PRJNA833581
(NCBI), accessed on 15 November 2023		35.62HV-30
AU merit cultivar		1.6292n = 14Illumina short-read NextSeq 500 WGS and Hi-C, PacBio HiFi sequencing
Sequel II platform		74 + 21 + 4318885373/13846049953,32181.8
Table 2. Summary of applications in biotic and abiotic stress studies using the genomic information from the Fabeae tribe. n.a. means not available.
Table 2. Summary of applications in biotic and abiotic stress studies using the genomic information from the Fabeae tribe. n.a. means not available.
SpeciesBiotic StressAbiotic Stress
TraitApproachReferencesTraitApproachReferences
P. sativum cv. CaméorPowdery mildew resistanceGWAS and comparative genomics[61,62,63]Drought toleranceGenotyping, GWAS, and proteomics[64,65,66,67,68]
White mold resistancecandidate genes identification[69]Heat toleranceGWAS, candidate genes identification, and proteomics[19,68,70]
Rust resistanceGWAS and comparative genomics[71,72]Frost toleranceCandidate genes identification and syntenic studies[73,74]
Ascochyta blight resistancecandidate genes identification Cold toleranceMapping of transcriptome and miRNA sequencing[75]
Fusarium wilt and root rot resistanceGWAS, QTL mapping, and candidate gene identification[76,77]Salinity toleranceMining ortholog genes and miRNAs[78]
Aphanomyces root rot resistanceSNP quality assessment, QTL mapping, and proteomics[79,80,81]
Aphid resistanceGWAS[82]
Bruchid resistanceQTL mapping and candidate gene identification[83]
Parasitic plant Orobanche crenata resistanceComparative mapping[20]
Herbivore resistanceCandidate gene identification[84]
V. faba cv. Hedin/2n.a.Drought toleranceTranscriptome analysis[85]
Drought and salt stressGene expression[86]
Drought tolerance (PRO and SPAD levels)GWAS[87]
L. culinarisAscochyta blight resistanceTranscriptome (RNA-seq) analysis[88]Salt stressGWAS[89]
Anthracnose race 1 resistanceGWAS[90]
Stemphylium blight resistanceGWAS[91]
Powdery mildew (MLO genes)GWAS[92]
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Santos, C.; Leitão, S.T. The Exceptionally Large Genomes of the Fabeae Tribe: Comparative Genomics and Applications in Abiotic and Biotic Stress Studies. Agriculture 2024, 14, 77. https://doi.org/10.3390/agriculture14010077

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Santos C, Leitão ST. The Exceptionally Large Genomes of the Fabeae Tribe: Comparative Genomics and Applications in Abiotic and Biotic Stress Studies. Agriculture. 2024; 14(1):77. https://doi.org/10.3390/agriculture14010077

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Santos, Carmen, and Susana Trindade Leitão. 2024. "The Exceptionally Large Genomes of the Fabeae Tribe: Comparative Genomics and Applications in Abiotic and Biotic Stress Studies" Agriculture 14, no. 1: 77. https://doi.org/10.3390/agriculture14010077

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