Banana breeding by genome design

Abstract

Bananas and plantains of the genus Musa constitute the most vital fruits and staple foods. Cultivated bananas may have originated from intraspecific and interspecific hybridizations of four wild species, namely Musa acuminata (A), M. balbisiana (B), M. schizocarpa (S), and the Australimusa species (T). Here, we appraise the advances made in banana genomics, genetics, and breeding over the past few decades. The sequencing of Musa genomes has been a major breakthrough in banana research programs, presenting unprecedented possibilities for gaining deeper insights into the evolution, domestication, breeding, and genetics of indispensable agronomic traits of bananas. Also, we delve into how these genetic facets, coupled with innovative genomic-assisted tools, including genomic selection and gene editing, propel advancements in banana breeding endeavors. Ultimately, we propose the forthcoming prospects within the domain of banana genetics and breeding.

Keywords: Musa; bananas; domestication; genetics; genomic breeding; genomics.

Figure 1

Phylogenetic relationships and evolutionary insights of Musa species and domesticated bananas (A) Phylogenetic tree illustrates the evolutionary relationships among Musa spp. and their wild relatives. (B) Evolution of domesticated bananas (adopted from Simmonds and Shepherd, 1955).

Figure 2

Origin and selection during domestication and improvement of bananas (A) Origins and global dispersal patterns of bananas across historical epochs: A holistic exploration (Mohandas and Ravishankar, 2016). (B) A schematic diagram rendering the phenotypic and genetic diversity during domestication and improvement of bananas. The domestication process of bananas has faced a weak bottleneck, leading to marginal diversity reduction, while the improvement process depicts a marked reduction in diversity.

Figure 3

Multi‐omics approaches for banana improvement (A) Schematic diagram of multi‐omics approaches, genetic improvement platforms, and tools for bananas. (B) Headway of genome sequencing for different Musa spp. over the last two decades. (C) Schematic diagram of various stages of genomic selection for banana improvement. GEBV, genomic estimated breeding value; QTLs, quantitative trait loci; T2T, telomere to telomere.

Figure 4

Genome engineering approaches for banana improvement and breeding through the manipulation of multiple genes (A) Introducing the TLP gene from rice into bananas to create a Foc1‐resistant transgenic cultivar (Mahdavi et al., 2012). (B) RNAi‐induced gene silencing to produce bananas with delayed ripening (Elitzur et al., 2016). (The genes modified for genetic improvement are indicated.) (C) Gene editing using the CRISPR/Cas9 technique to design semi‐dwarf bananas (Shao et al., 2020), and bananas with extended shelf life(Hu et al., 2021) and β‐carotene enrichment (Kaur et al., 2020). CRISPR/Cas9, Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR‐associated protein 9; Foc1, Fusarium oxysporum f. sp. Cubense race 1; gRNA, guide RNA; RNAi, RNA interference; RISC, RNA‐induced silencing complex; T‐DNA, transfer DNA.

Figure 5

A sneak peek at the future Ascertaining beneficial and deleterious alleles within banana genetic resources can be expedited by using pangenomics, GWAS, and population genetics analyses. Novel adaptive or exotic alleles undergo additional steps for the efficient, accurate, and specific modification of important traits. Gene editing and genome design are powerful techniques that can serve to retain beneficial alleles while removing deleterious mutations in bananas (e.g., disease resistance). Haplotype‐based breeding relies on a specific group of important genes, while breeding techniques like genomic selection are expected to mitigate the genetic diversity within a breeding program over time. Advancements occurring concomitantly in image and sensor technologies will enable the acquisition of highly accurate phenotyping data. Integrating these tools with AI‐based approaches leads to intelligent breeding—referred to as Breeding 4.0—which unifies the advanced genomic technologies, high‐throughput phenotyping, and data‐driven computational approaches to accelerate and optimize crop development. This holistic strategy will facilitate the creation of superior banana cultivars critical for future food security. CRISPR/Cas9, Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR‐associated protein 9; GEBV, Genomic estimated breeding value; gRNA, guide RNA; GWAS, Genome‐Wide Association Studies; InDels, Insertions and deletions; SNP, Single nucleotide polymorphism; SV, Structural variations.