1 Introduction

Lupinus species, commonly known as lupins, are significant grain legume crops that play a crucial role in sustainable farming systems. They are known for their ability to fix atmospheric nitrogen, which reduces the need for synthetic fertilizers and improves soil health (Hane et al., 2016). Lupins are also valued for their high protein and dietary fiber content, making them a nutritious food source for both humans and livestock (Valente et al., 2023). The adaptability of lupins to a wide range of edaphoclimatic conditions further enhances their agricultural importance, allowing them to thrive in environments where other crops may not be viable (Martin et al., 2014; Msaddak et al., 2023).

Genomics, the study of an organism's complete set of DNA, including all of its genes, has revolutionized crop improvement by providing insights into the genetic basis of important traits (Zhou and Chen, 2024). Advances in genomic technologies, such as whole genome sequencing and the development of genetic linkage maps, have enabled researchers to identify genes associated with key agronomic traits, such as disease resistance, yield, and stress tolerance (Yang et al., 2013; Garg et al., 2022). In lupins, genomic studies have revealed significant information about their evolutionary history, gene families, and the mechanisms underlying their unique traits, such as nonmycorrhizal phosphorus acquisition and nitrogen fixation (Lambers et al., 2013; Czyż et al., 2020). These insights are critical for developing improved lupin cultivars with enhanced productivity and resilience.

This study conducts a comparative genomic analysis of various species of Lupinus to identify genetic factors for crop improvement, uncovering candidate genes associated with desirable traits such as high protein content, disease resistance, and environmental adaptability, including the sequencing and analysis of the Lupinus genome, identification of key genetic markers, and exploration of gene expression patterns related to important agronomic traits, with the aim of providing valuable genomic resources to accelerate Lupinus breeding programs and contribute to the development of superior Lupinus varieties for sustainable agriculture.

2 Genomic Diversity in Lupinus Species

2.1 Overview of the Lupinus genus and its species

The Lupinus genus, commonly known as lupins, comprises a diverse group of leguminous plants known for their high protein content and adaptability to various environmental conditions. Lupins are cultivated globally, with species such as Lupinus angustifolius (narrow-leafed lupin), Lupinus albus (white lupin), and Lupinus mutabilis (Andean lupin) being of significant agricultural importance. These species are valued not only for their nutritional benefits but also for their role in sustainable farming practices, such as nitrogen fixation and soil improvement (Guilengue et al., 2019; Msaddak et al., 2023).

2.2 Genetic diversity and its role in adaptation

Genetic diversity within Lupinus species plays a crucial role in their ability to adapt to different environmental conditions. For instance, Lupinus mutabilis exhibits significant genetic and phenotypic variability, which is essential for its adaptation to Mediterranean climates and other regions outside its native Andean environment (Figure 1) (Gulisano et al., 2022). Similarly, the genetic diversity observed in narrow-leafed lupin (Lupinus angustifolius) has been pivotal in its domestication and adaptation to various photoperiods and vernalization requirements (Taylor et al., 2018; Rychel-Bielska et al., 2020). The presence of diverse genetic traits, such as flowering time and yield components, enables the selection of accessions suited to specific environments, thereby enhancing crop performance and resilience (Gulisano et al., 2023).

2.3 Comparative genomics: current research and findings

Recent advances in comparative genomics have provided deeper insights into the genomic diversity and evolutionary history of Lupinus species. The development of a chromosome-length reference genome and pan-genome assembly for narrow-leafed lupin has revealed significant genomic variations, including the absence of essential mycorrhizal-associated genes and the presence of key alkaloid regulatory genes (Garg et al., 2022). Comparative studies between Lupinus species and other legumes have highlighted unique genomic features, such as the loss of mycorrhiza-specific genes in narrow-leafed lupin, which distinguishes it from other legumes (Hane et al., 2016).

Furthermore, epigenomic studies have uncovered variations in chromatin modifications and DNA methylation patterns among different Lupinus species, providing insights into their evolutionary processes and gene expression regulation (Susek et al., 2017). These findings underscore the importance of genomic and epigenomic diversity in the adaptation and evolution of Lupinus species, offering valuable resources for crop improvement and breeding programs.

The principal component analysis (PCA) depicted provides insights into the genetic diversity and performance of Lupinus mutabilis accessions across different environments. The distribution of accessions in relation to traits like seed yield, biomass, and pod formation highlights the variability in response to specific environments, such as Ecuador, Portugal, and northern Europe. Accessions with higher biomass yields in European trials are marked in red, demonstrating their potential for breeding programs aimed at improving yield under European conditions. This analysis helps in identifying traits and genotypes that are well-suited for specific climates and farming systems.

3 Comparative Genomics in Lupinus

3.1 Methods used in comparative genomics for Lupinus

Comparative genomics in Lupinus species has employed a variety of advanced techniques to elucidate genetic differences and similarities. Key methods include genome-wide association studies (GWAS), which have been used to identify single nucleotide polymorphisms (SNPs) associated with important agronomic traits in Lupinus mutabilis. Whole-genome sequencing and pan-genome assembly have also been pivotal, as demonstrated by the creation of a chromosome-length reference genome for narrow-leafed lupin (Lupinus angustifolius) and the comparison with white lupin (Lupinus albus). Additionally, epigenomic studies using immunostaining of methylated histone H3 and DNA methylation, as well as whole-genome bisulfite sequencing, have provided insights into the epigenetic landscape of various Lupinus species (Susek et al., 2017). Transcriptome sequencing and the development of expressed sequence tag (EST) libraries have further facilitated comparative studies and marker development (Parra-González et al., 2012).

3.2 Key genomic features identified in different Lupinus species

Several key genomic features have been identified across different Lupinus species. In Lupinus angustifolius, the discovery of natural mutations conferring vernalization independence, such as the Ku and Jul alleles, has been significant for understanding flowering time regulation (Figure 2) (Rychel-Bielska et al., 2020). The genome of L. angustifolius also revealed the absence of essential mycorrhizal-associated genes, which is unique among legumes. In Lupinus luteus, comparative mapping has highlighted syntenic regions with major orthologous genes controlling anthracnose resistance and flowering time, suggesting the presence of orthologous genes for these traits in the L. luteus genome. For Lupinus mutabilis, genetic and genomic diversity studies have identified significant intra-specific variability, which is crucial for breeding and conservation programs (Guilengue et al., 2019). Additionally, genome-wide association studies in L. mutabilis have pinpointed QTLs linked to vegetative yield, plant height, pods number, and flowering time (Gulisano et al., 2023).

3.3 Implications of genetic variations for crop improvement

The genetic variations identified in Lupinus species have profound implications for crop improvement. The identification of vernalization-independent alleles in L. angustifolius can lead to the development of early-flowering varieties, which are advantageous for different climatic conditions. The absence of mycorrhizal-associated genes in L. angustifolius suggests a unique adaptation mechanism that could be exploited for breeding programs aimed at enhancing nutrient uptake efficiency (Garg et al., 2022). The syntenic regions identified in L. luteus for anthracnose resistance and flowering time can be targeted for marker-assisted selection to develop disease-resistant and early-flowering cultivars (Lichtin et al., 2020). The genetic diversity observed in L. mutabilis provides a rich resource for selecting high-yielding and well-adapted varieties for European climates, thereby expanding its cultivation beyond its native Andean region (Gulisano et al., 2022). Overall, these genetic insights facilitate the development of improved Lupinus varieties with enhanced yield, disease resistance, and adaptability to diverse environmental conditions.

4 Genomic Tools and Technologies

4.1 Genome sequencing and assembly in Lupinus species

Genome sequencing and assembly have been pivotal in advancing our understanding of Lupinus species. For instance, the draft genome sequence of Lupinus angustifolius was constructed using whole genome shotgun sequencing, achieving a 26.9x coverage and predicting 57 807 genes. This assembly, combined with a high-density genetic linkage map, facilitated the identification of functional genes of agronomic interest, such as those associated with disease resistance (Yang et al., 2013). Additionally, the construction of an ultra-high density consensus genetic map containing 34 574 sequence-defined markers has significantly enhanced the physical map, covering 560.5 Mb of the genome sequence (Zhou et al., 2017). These genomic resources are crucial for structural genomics, comparative genomics, and molecular plant breeding.

4.2 Genomic markers and their application in breeding

Genomic markers are essential tools in molecular breeding, enabling the identification and selection of desirable traits. In Lupinus luteus, transcriptome sequencing has led to the development of a comprehensive set of EST-simple sequence repeat (SSR) markers, which have been validated for their utility in diversity studies and transferability to related species (Parra-González et al., 2012). Similarly, in Lupinus angustifolius, whole genome re-sequencing has been employed to develop diagnostic DNA markers tightly linked to disease-resistance loci, facilitating marker-assisted selection (Yang et al., 2015). The application of next-generation sequencing (NGS) technologies, such as RAD sequencing, has further accelerated marker development, enabling the rapid identification of SNP markers linked to disease resistance genes (Yang et al., 2012).

4.3 CRISPR and gene-editing technologies in Lupinus research

CRISPR/Cas9 technology has revolutionized functional genomics and crop improvement by enabling precise genetic modifications (Guo, 2024). In Lupinus albus, the CRISPR/Cas9 system has been adapted for multiplex genome editing using endogenous promoters, achieving high mutation frequencies in target genes (Zhu et al., 2023). This technology has the potential to enhance traits such as disease resistance, nutritional quality, and stress tolerance. The broader application of CRISPR/Cas9 in plant breeding includes generating knockouts, making precise modifications, and fine-tuning gene regulation, which are critical for developing improved crop varieties (Arora and Narula, 2017; Chen et al., 2019). The integration of CRISPR/Cas9 with traditional breeding methods promises to accelerate the development of superior lupin cultivars.

5 Insights into Agronomic Traits

5.1 Genetic basis of drought and stress resistance

Drought and stress resistance are critical traits for the successful cultivation of lupin species, particularly in regions prone to water scarcity. Research on white lupin (Lupinus albus) has identified significant genetic variation and genotype × environment interactions for grain yield and other traits under drought conditions. A genome-wide association study (GWAS) using 9 828 SNP markers revealed that yield under drought conditions is polygenic and heritable, with a high predictive ability for genomic selection models. Notably, two significant QTLs for yield were identified, which differed between drought-prone and moisture-favorable conditions, highlighting the complex genetic architecture of drought tolerance (Pecetti et al., 2023). Additionally, narrow-leafed lupin (Lupinus angustifolius) has been shown to possess genes associated with abiotic stress tolerance, including drought and heat, which are crucial for maintaining high yield under adverse environmental conditions (Plewiński et al., 2020).

5.2 Nutritional content and quality improvement

Lupin species are valued for their high protein and dietary fiber content, making them an excellent alternative to traditional protein sources like soybean. The draft genome sequence of narrow-leafed lupin has provided insights into the amino acid profile of storage proteins in seeds, which are essential for nutritional quality improvement (Yang et al., 2013). Furthermore, the pan-genome assembly of narrow-leafed lupin has identified key alkaloid regulatory genes, such as LaRAP2-7, which are important for reducing anti-nutritional factors and enhancing the overall quality of lupin seeds (Garg et al., 2022). The genetic resources generated from these studies offer new opportunities to fast-track lupin crop improvement, focusing on enhancing nutritional content and quality (Hane et al., 2016).

5.3 Disease resistance: genomic insights and breeding strategies

Disease resistance is a major focus in lupin breeding programs, given the susceptibility of lupin species to various pathogens. The genetic mapping of Lupinus luteus has revealed syntenic regions with major orthologous genes controlling anthracnose resistance, a significant disease affecting lupin yield. The study identified QTLs for anthracnose resistance, with marker sequences flanking these QTLs showing high homology with the Lanr1 gene of Lupinus angustifolius, suggesting the presence of orthologous resistance genes in L. luteus (Lichtin et al., 2020). Similarly, the draft genome sequence of narrow-leafed lupin has facilitated the identification of candidate R genes associated with resistance to anthracnose, demonstrating the potential of genomic tools in enhancing disease resistance through marker-assisted selection. Additionally, the high-density consensus linkage map of white lupin has mapped QTLs for resistance to anthracnose and Phomopsis stem blight, providing markers that are immediately applicable for breeding programs (Książkiewicz et al., 2017).

6 Case Study

6.1 Introduction to the selected case study: Lupinus albus (white lupin)

Lupinus albus, commonly known as white lupin, is a leguminous plant recognized for its high protein content and ability to thrive in poor soils. It has been cultivated since ancient times and is valued for its use as green manure, cover crop, and for its seeds, which are rich in protein and oil. White lupin is particularly noted for its ability to grow in phosphorus-deficient soils due to its unique root adaptations (Wang et al., 2014).

6.2 Genomic research on Lupinus albus and key findings

Recent genomic studies on Lupinus albus have provided significant insights into its genetic structure and adaptive mechanisms. One study highlighted the genetic diversity within a USDA germplasm collection, identifying markers associated with seed weight variation and demonstrating the potential for association mapping in breeding programs (Iqbal et al., 2012). Another research effort focused on the quantitative control of early flowering, identifying key QTLs and regulatory genes involved in flowering time, which is crucial for adapting the crop to different climates (Rychel-Bielska et al., 2021). Additionally, the genome of white lupin has been sequenced, revealing its evolution from a whole-genome triplication event and identifying pathways for high phosphorus-use efficiency. Transcriptome sequencing has further elucidated the regulatory networks involved in cluster root development and function, which are essential for phosphate acquisition.

6.3 Practical applications of genomic insights for crop improvement in specific regions

The genomic insights gained from studies on Lupinus albus have several practical applications for crop improvement, particularly in regions with challenging growing conditions. For instance, the identification of genetic markers associated with seed weight and flowering time can be used to develop high-yielding, early-flowering varieties suitable for diverse climates. In regions with phosphorus-deficient soils, the understanding of cluster root development and phosphate acquisition mechanisms can inform breeding programs aimed at enhancing phosphorus-use efficiency (Xu et al., 2020). Additionally, the adaptation of CRISPR/Cas9 technology for genome editing in white lupin opens new avenues for precise genetic modifications to improve traits such as disease resistance and nutrient uptake (Zhu et al., 2023).

6.4 Lessons learned and implications for other Lupinus species

The research on Lupinus albus provides valuable lessons for the improvement of other Lupinus species. The methodologies and findings related to genetic diversity, marker-trait associations, and genome sequencing can be applied to other species to enhance their breeding programs. For example, the insights into flowering time control and phosphorus-use efficiency in white lupin can guide similar studies in narrow-leafed lupin (Lupinus angustifolius) and other related species (Garg et al., 2022; Spina et al., 2022). Furthermore, the successful application of CRISPR/Cas9 technology in white lupin suggests that similar approaches could be used to accelerate genetic improvements in other Lupinus species. Overall, the comparative genomics of Lupinus species holds great promise for advancing crop improvement and ensuring sustainable agricultural practices.

7 Challenges and Future Perspectives

7.1 Current limitations in Lupinus genomics research

Lupinus genomics research faces several significant challenges. One of the primary limitations is the relatively recent domestication of key species such as Lupinus angustifolius, which has resulted in a limited understanding of its genetic diversity and functional genomics (Yang et al., 2013). Additionally, the absence of essential mycorrhizal-associated genes in narrow-leafed lupin (NLL) complicates the study of plant-microbe interactions, which are crucial for nutrient uptake and stress resistance (Garg et al., 2022). The genomic resources for some Lupinus species, such as Lupinus luteus, are still underdeveloped, limiting the ability to perform comprehensive comparative studies and marker-assisted selection (Parra-González et al., 2012). Furthermore, the high level of genomic diversity within species like Lupinus mutabilis presents a challenge for breeding programs aimed at improving crop traits (Guilengue et al., 2019).

7.2 Potential strategies for overcoming genomic challenges

To overcome these challenges, several strategies can be employed. First, expanding the genomic resources through whole genome sequencing and re-sequencing can provide a more comprehensive understanding of genetic diversity and facilitate the development of diagnostic markers for molecular breeding (Yang et al., 2015). The integration of high-density genetic linkage maps with genome sequencing data can help identify and study functional genes of agronomic interest, such as those related to disease resistance and flowering time (Lichtin et al., 2020). Additionally, leveraging comparative genomics with model legume species can reveal syntenic regions and orthologous genes, aiding in the identification of candidate genes for important traits (Książkiewicz et al., 2013). The use of advanced sequencing technologies, such as RNA sequencing and expression quantitative trait loci (eQTL) mapping, can further elucidate the regulatory networks controlling key phenotypes, such as alkaloid biosynthesis and vernalization response (Plewiński et al., 2019).

7.3 Future directions for crop improvement through comparative genomics

Future research in Lupinus genomics should focus on several key areas to enhance crop improvement. One promising direction is the development of pan-genomes for multiple Lupinus species, which can capture the full spectrum of genetic diversity and identify core and variable genes essential for breeding programs. Comparative genomics studies should be expanded to include a broader range of Lupinus species and their close relatives, providing insights into legume evolution and the genetic basis of important traits (Hane et al., 2016). Additionally, the identification and functional characterization of genes involved in stress resistance, nutrient uptake, and symbiotic interactions can lead to the development of more resilient and high-yielding lupin varieties (Msaddak et al., 2023). Finally, the application of marker-assisted selection and genomic selection techniques can accelerate the breeding process, enabling the rapid development of improved cultivars with desirable traits such as disease resistance, early flowering, and high protein content.

8 Concluding Remarks

The comparative genomics of various Lupinus species has revealed significant insights into their genetic and genomic diversity, which are crucial for crop improvement. The narrow-leafed lupin (Lupinus angustifolius) has been extensively studied, with a chromosome-length reference genome and a pan-genome assembly highlighting the core and variable genes, as well as the absence of essential mycorrhizal-associated genes. The draft genome sequence of L. angustifolius has captured over 98% of the gene content and identified candidate genes for key disease resistance and domestication traits. Epigenomic studies have shown variations in chromatin modifications among different Lupinus species, providing insights into their evolutionary processes. Additionally, genetic and genomic diversity studies in Lupinus mutabilis have identified significant intra-specific variability, which is essential for breeding and conservation programs. Genome-wide association studies have pinpointed QTLs linked to important agronomic traits, facilitating marker-assisted selection. Cytogenetic mapping has revealed karyotype variations and chromosomal rearrangements, contributing to our understanding of lupin genome evolution.

The genomic resources generated for Lupinus species offer new opportunities to fast-track crop improvement. The identification of core and variable genes, as well as candidate genes for disease resistance and domestication traits, provides a solid foundation for developing improved lupin varieties. The absence of mycorrhizal-associated genes in L. angustifolius suggests a unique adaptation mechanism that could be leveraged for breeding programs. The epigenomic diversity observed among Lupinus species can be exploited to understand gene expression regulation and its impact on phenotypic traits, aiding in the selection of desirable traits. The genetic diversity within L. mutabilis and the identification of QTLs for agronomic traits are pivotal for developing varieties adapted to different environmental conditions, particularly in Europe. The cytogenetic insights into karyotype evolution and chromosomal rearrangements provide a framework for understanding the genetic basis of important traits and for developing chromosome-specific markers for breeding.

Acknowledgments

Thanks to the anonymous peer review for their critical comments and revising suggestion.

Conflict of Interest Disclosure

The author affirms that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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