The biomass demand to fuel a growing global bio-based economy is expected to tremendously increase over the next decades, and projections indicate that dedicated biomass crops will satisfy a large portion of it. The establishment of dedicated biomass crops raises huge concerns, as they can subtract land that is required for food production, undermining food security. In this context, perennial biomass crops suitable for cultivation on marginal lands (MALs) raise attraction, as they could supply biomass without competing for land with food supply. While these crops withstand marginal conditions well, their biomass yield and quality do not ensure acceptable economic returns to farmers and cost-effective biomass conversion into bio-based products, claiming genetic improvement. However, this is constrained by the lack of genetic resources for most of these crops. Here we first review the advantages of cultivating novel perennial biomass crops on MALs, highlighting management practices to enhance the environmental and economic sustainability of these agro-systems. Subsequently, we discuss the preeminent breeding targets to improve the yield and quality of the biomass obtainable from these crops, as well as the stability of biomass production under MALs conditions. These targets include crop architecture and phenology, efficiency in the use of resources, lignocellulose composition in relation to bio-based applications, and tolerance to abiotic stresses. For each target trait, we outline optimal ideotypes, discuss the available breeding resources in the context of (orphan) biomass crops, and provide meaningful examples of genetic improvement. Finally, we discuss the available tools to breed novel perennial biomass crops. These comprise conventional breeding methods (recurrent selection and hybridization), molecular techniques to dissect the genetics of complex traits, speed up selection, and perform transgenic modification (genetic mapping, QTL and GWAS analysis, marker-assisted selection, genomic selection, transformation protocols), and novel high-throughput phenotyping platforms. Furthermore, novel tools to transfer genetic knowledge from model to orphan crops (i.e., universal markers) are also conceptualized, with the belief that their development will enhance the efficiency of plant breeding in orphan biomass crops, enabling a sustainable use of MALs for biomass provision.

Translational genomics can enable a quicker improvement of orphan crops toward novel agricultural applications, including the advancement of orphan biomass species for cultivation on marginal lands. In this sense, cell wall quality is a preeminent breeding target. However, tools to efficiently project genetic data on target traits across large sets of species are currently missing. This study aimed at closing this gap by developing a strategy to project a set of cell wall QTLs across a large group of plants by using genome synteny. This strategy is suited for large-scale analyses and detected 362 syntenic cell wall QTLs (SQTLs) across 74 angiosperms, including several (orphan) biomass species. SQTLs analyses revealed that they span large portions of the initial cell wall QTLs and are extensively conserved across diverse species. Moreover, numerous QTLs cell wall genes were conserved through SQTLs, including genes displaying allelic variation associated with cell wall composition. Functional analyses showed that highly conserved genes of SQTLs include important cell wall transcription factors and genes involved in the remodeling of cell wall polymers. For some of these gene families, SQTLs indicated the presence of differentially conserved genomic contexts for different gene members, highlighting their utility as a tool to pinpoint gene targets that maximize the likelihood of functional gene conservation. Overall, the results of this study can facilitate “universal” approaches for breeding (orphan) biomass crops, while the strategy for QTLs translation can be applied to other sets of traits and species, helping to unlock the potential of orphan species.

The Cellulose synthase superfamily synthesizes cellulose and different hemicellulosic polysaccharides in plant cell walls. While much has been discovered about the evolution and function of these genes, their genomic architecture and relationship with gene (sub-)functionalization and evolution remains unclear. By using 242 genomes covering plant evolution from green algae to eudicots, we performed a large-scale analysis of synteny, phylogenetic, and functional data of the CesA superfamily. Results revealed considerable gene copy number variation across species and gene families, and also two patterns – singletons vs. tandem arrays – in chromosomic gene arrangement. Synteny analysis revealed exceptional conservation of gene architecture across species, but also lineage-specific patterns across gene (sub-)families. Synteny patterns correlated with gene sub-functionalization into primary and secondary CesAs and distinct CslD functional isoforms. Furthermore, a genomic context shift of a group of cotton secondary CesAs was associated with peculiar properties of cotton fiber synthesis. Finally, phylogenetics suggested that primary CesA sequences appeared before the secondary CesAs, while phylogenomic analyses unveiled the genomic trace of the CslD duplication that initiated the CslF family. Our results describe in detail the genomic architecture of the CesA superfamily in plants, highlighting its crucial relevance for gene diversification and sub-functionalization, and for understanding their evolution.

Syntenic cell wall QTLs (SQTLs) can identify genetic determinants of biomass traits in understudied species based on results from model crops. However, their effective use in plant breeding requires SQTLs to display intraspecific allelic variability and to predict causative loci in other populations/species than the ones used for SQTLs identification. In this study, genome assemblies from different accessions of Arabidopsis, rapeseed, tomato, rice, Brachypodium and maize were used to evaluate the intraspecific variability of SQTLs. In parallel, a genome-wide association study (GWAS) on cell wall quality traits was performed in miscanthus to verify the colocalization between GWAS loci and miscanthus SQTLs. Finally, an analogous approach was applied on a set of switchgrass cell wall QTLs retrieved from the literature. These analyses revealed large SQTLs intraspecific genetic variability, ranging from presence–absence gene variation to SNPs/INDELs and changes in coded proteins. Cell wall genes displaying gene dosage regulation, such as PAL and CAD, displayed presence–absence variation in Brachypodium and rapeseed, while protein INDELs were detected for the Brachypodium homologs of the rice brittle culm-like 8 locus, which may likely impact cell wall quality. Furthermore, SQTLs significantly colocalized with the miscanthus and switchgrass QTLs, with relevant cell wall genes being retained in colocalizing regions. Overall, SQTLs are useful tools to screen germplasm for relevant genes and alleles to improve biomass quality and can increase the efficiency of plant breeding in understudied biomass crops.

The Cellulose synthase superfamily synthesizes cellulose and different hemicellulosic polysaccharides in plant cell walls. While much has been discovered about the evolution and function of these genes, their genomic architecture and its relationship with gene (sub-)functionalization and evolution remains unclear. By using 242 genomes covering plant evolution from green algae to eudicots, we performed a largescale analysis of synteny, phylogenetic, and functional data of the CesA superfamily. Results revealed considerable gene copy number variation across species and gene families, as well as two patterns -singletons vs tandem arrays -in chromosomic gene arrangement. Synteny analysis revealed exceptional conservation of gene architecture across species, but also lineage-specific patterns across gene (sub-)families. Synteny patterns correlated with gene sub-functionalization into primary and secondary CesAs and distinct CslD functional isoforms. Furthermore, a genomic context shift of a group of cotton secondary CesAs was associated with peculiar properties of cotton fiber synthesis. Finally, phylogenetics suggested that primary CesA sequences appeared before the secondary CesAs, while phylogenomic analyses unveiled the genomic trace of the CslD duplication that initiated the CslF family. Our results describe in detail the genomic architecture of the CesA superfamily in plants, highlighting its crucial relevance for gene diversification and sub-functionalization, and for understanding their evolution.