The narrow genetics of most crops is a fundamental vulnerability to food security. This makes wild crop relatives a strategic resource of genetic diversity that can be used for crop improvement and adaptation to new agricultural challenges. Here, we uncover the contribution of one wild species accession, Arachis cardenasii GKP 10017, to the peanut crop (Arachis hypogaea) that was initiated by complex hybridizations in the 1960s and propagated by international seed exchange. However, until this study, the global scale of the dispersal of genetic contributions from this wild accession had been obscured by the multiple germplasm transfers, breeding cycles, and unrecorded genetic mixing between lineages that had occurred over the years. By genetic analysis and pedigree research, we identified A. cardenasii–enhanced, disease-resistant cultivars in Africa, Asia, Oceania, and the Americas. These cultivars provide widespread improved food security and environmental and economic benefits. This study emphasizes the importance of wild species and collaborative networks of international expertise for crop improvement. However, it also highlights the consequences of the implementation of a patchwork of restrictive national laws and sea changes in attitudes regarding germplasm that followed in the wake of the Convention on Biological Diversity. Today, the botanical collections and multiple seed exchanges which enable benefits such as those revealed by this study are drastically reduced. The research reported here underscores the vital importance of ready access to germplasm in ensuring long-term world food security. Significance A great challenge for humanity is feeding its growing population while minimizing ecosystem damage and climate change. Here, we uncover the global benefits arising from the introduction of one wild species accession to peanut-breeding programs decades ago. This work emphasizes the importance of biodiversity to crop improvement: peanut cultivars with genetics from this wild accession provided improved food security and reduced use of fungicide sprays. However, this study also highlights the perilous consequences of changes in legal frameworks and attitudes concerning biodiversity. These changes have greatly reduced the botanical collections, seed exchanges, and international collaborations which are essential for the continued diversification of crop genetics and, consequently, the long-term resilience of crops against evolving pests and pathogens and changing climate.

Premise of the Study: The genetic bottleneck of polyploid formation can be mitigated by multiple origins, gene flow, and recombination among different lineages. In crop plants with limited origins, efforts to increase genetic diversity have limitations. Here we used lineage recombination to increase genetic diversity in peanut, an allotetraploid likely of single origin, by crossing with a novel allopolyploid genotype and selecting improved lines.Methods: Single backcross progeny from cultivated peanut × wild species‐derived allotetraploid cross were studied over successive generations. Using genetic assumptions that encompass segmental allotetraploidy, we used single nucleotide polymorphisms and whole‐genome sequence data to infer genome structures.Key Results: Selected lines, despite a high proportion of wild alleles, are agronomically adapted, productive, and with improved disease resistances. Wild alleles mostly substituted homologous segments of the peanut genome. Regions of dispersed wild alleles, characteristic of gene conversion, also occurred. However, wild chromosome segments sometimes replaced cultivated peanut's homeologous subgenome; A. ipaënsis B sometimes replaced A. hypogaea A subgenome (~0.6%), and A. duranensis replaced A. hypogaea B subgenome segments (~2%). Furthermore, some subgenome regions historically lost in cultivated peanut were “recovered” by wild chromosome segments (effectively reversing the “polyploid ratchet”). These processes resulted in lines with new genome structure variations.Conclusions: Genetic diversity was introduced by wild allele introgression, and by introducing new genome structure variations. These results highlight the special possibilities of segmental allotetraploidy and of using lineage recombination to increase genetic diversity in peanut, likely mirroring what occurs in natural segmental allopolyploids with multiple origins.

Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.

The introduction of genes from wild species is a practice little adopted by breeders for the improvement of commercial crops, although it represents an excellent opportunity to enrich the genetic basis and create new cultivars. In peanut, this practice is being increasingly adopted. In this study we present results of introgression of wild alleles from the wild species Arachis duranensis and A. batizocoi improving photosynthetic traits and yield in a set of lines derived from the cross of an induced allotetraploid and cultivated peanut with selection under water stress. The assays were carried out in greenhouse and field focusing on physiological and agronomic traits. A multivariate model (UPGMA) was adopted in order to classify drought tolerant lines. Several lines showed improved levels of tolerance, with values similar to or greater than the tolerant control. Two BC₁F₆ lines (53 P4 and 96 P9) were highlighted for good drought-related traits, earliness and pod yield, having better phenotypic profile to the drought tolerant elite commercial cultivar BR1. These lines are good candidates for the creation of peanut cultivars suitable for production in semiarid environments.

Root-knot nematode is a very destructive pathogen, to which most peanut cultivars are highly susceptible. Strong resistance is present in the wild diploid peanut relatives. Previously, QTLs controlling nematode resistance were identified on chromosomes A02, A04 and A09 of Arachis stenosperma. Here, to study the inheritance of these resistance alleles within the genetic background of tetraploid peanut, an F₂ population was developed from a cross between peanut and an induced allotetraploid that incorporated A. stenosperma, [Arachis batizocoi x A. stenosperma]^4×. This population was genotyped using a SNP array and phenotyped for nematode resistance. QTL analysis allowed us to verify the major-effect QTL on chromosome A02 and a secondary QTL on A09, each contributing to a percentage reduction in nematode multiplication up to 98.2%. These were validated in selected F_2:3 lines. The genome location of the large-effect QTL on A02 is rich in genes encoding TIR-NBS-LRR protein domains that are involved in plant defenses. We conclude that the strong resistance to RKN, derived from the diploid A. stenosperma, is transferrable and expressed in tetraploid peanut. Currently it is being used in breeding programs for introgressing a new source of nematode resistance and to widen the genetic basis of agronomically adapted peanut lines.

Wild relatives of peanut harbor alleles that confer strong resistance to diseases and pests and adaptation to environmental stresses, traits that frequently cannot be found in Arachis hypogaea. However, most wild species are diploid, while cultivated peanut (A. hypogaea L.) is tetraploid. When crossed, they produce sterile progeny, thus hindering their direct use in peanut breeding. To make the alleles of three wild species accessions directly available for breeding, we developed at the University of Georgia two fertile artificially induced allotetraploids (also known as amphidiploids or neotetraploids): GA‐BatSten1 (Reg. no. GP‐239, PI 695418) and GA‐MagSten1 (GP‐240, PI 695417). They derive from crosses between wild diploid species of peanut, A. batizocoi × A. stenosperma, and A. magna × A. stenosperma, respectively. Cuttings from the sterile diploid F₁s were treated with colchicine. From some of these cuttings, fertile induced tetraploid seed were produced. These induced tetraploids are compatible with cultivated peanut, carry resistance to early and late leaf spot and root‐knot nematode, and are being used in breeding programs in the United States for the production of resistant cultivars.