Phylogenomic discovery of deleterious mutations facilitates hybrid potato breeding

Wu, Yaoyao; Li, Dawei; Hu, Yong; Li, Hongbo; Ramstein, Guillaume P.; Zhou, Shaoqun; Zhang, Xinyan; Bao, Zhigui; Song, Baoxing; Zhou, Yao; Zhou, Yongfeng; Gagnon, Edeline; Särkinen, Tiina; Knapp, Sandra; Zhang, Chengqi; Städler, Thomas; Buckler, Edward S.; Huang, Sanwen

doi:10.1016/j.cell.2023.04.008

Cited by 19 publications

(20 citation statements)

References 120 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Recent resequencing studies have revealed that tetraploid cultivars exhibit a higher of deleterious mutations compared to diploid clones (Lian et al, 2019). However, they also exhibit a lower level of homozygous deleterious mutations (or expressed burden) due to inter-homolog complementation (Wu et al, 2023). Those findings agree with the often-reported correlation between heterozygosity and good field performances in potato (Mendoza and Haynes, 1974).…”

Section: Key Differences Between Breeding Strategiessupporting

confidence: 79%

“…Another point of concern is that the removal of large-effect deleterious mutations does not eliminate inbreeding depression as a whole. Low vigour can also result from the cumulative effect of many mildly deleterious alleles (Charlesworth and Willis, 2009;Wu et al, 2023;Zhang et al, 2021). The challenge of identifying and removing such minor-effect deleterious mutations is comparable to the challenge of identifying and combining the multitude of minor-effect QTLs underlying complex quantitative traits.…”

Section: Selfing Of Diploids Results In the Loss Of Vigour And Fertilitymentioning

confidence: 99%

See 1 more Smart Citation

Natural variation in potato sexual reproduction facilitates breeding

Clot

View full text Add to dashboard Cite

The origin and widespread occurrence of Sli based self-compatibility in potato Chapter 3 46 High-density linkage map constructed from a skim sequenced diploid potato population reveals transmission distortion and QTLs for tuber yield and pollen shed Chapter 4 74Desynapsis in potato is caused by StMSH4 mutant alleles and leads to either highly uniform unreduced pollen or sterility Chapter 5 94Identification of two mutant JASON-RELATED genes associated with unreduced pollen production in potato Chapter 6 122 General discussion References 143Summary 167Acknowledgements 171 About the author 179Education statement recognition model (Kubo et al., 2010), the combined action of the SLFs encoded by one S-haplotype results in the recognition and degradation of all S-RNases except of the one encoded by their own haplotype. Hence, self-incompatibility occurs when the Shaplotype of the pollen matches either of the two S-haplotypes of the style. This elegant model also provides an explanation for the phenomenon of competitive interaction that allows tetraploid potatoes to become self-compatible (Olsder and Hermsen, 1976). When tetraploid clones produce diploid heteroallelic pollen that expresses two complementary sets of S-locus F-box proteins (SLFs), all S-RNases are ubiquitinated, which breaks down gametophytic self-incompatibility.Recently, self-compatible diploid potato clones were engineered by a knock-out of the gene encoding for the S-RNase (Enciso-Rodriguez et al., 2019;Ye et al., 2018). Furthermore, a self-compatible diploid clone bearing a naturally weakly expressed S-RNase was recently identified . Other cases of self-compatibility among S. tuberosum dihaploids were reported in earlier studies (De Jong and Rowe, 1971;Olsder and Hermsen, 1976), but the genetic and mechanistic basis of their selfcompatibility remained undetermined prior to this thesis. Despite those alternative options, the most widely used source of self-compatibility is the dominant gene Sli originally identified from a S. chacoense accession and located on chromosome 12 Hanneman, 1998a, 1998b). The causal gene behind Sli was recently shown to encode for a pollen-expressed F-box protein functioning as a general S-RNase inhibitor (Eggers et al., 2021;Ma et al., 2021).

show abstract

Section: Key Differences Between Breeding Strategiessupporting

confidence: 79%

Section: Selfing Of Diploids Results In the Loss Of Vigour And Fertilitymentioning

confidence: 99%

Natural variation in potato sexual reproduction facilitates breeding

Clot

View full text Add to dashboard Cite

show abstract

“…Building up this general framework is a step towards inference methods that coherently integrate intra- and interspecific variation to understand the genotype-to-phenotype map and how evolutionary processes, acting at different time scales, shape it. Indeed, the importance of evolutionary conservation in triaging functional variants in the human genome has long been appreciated and is becoming increasingly important as we collect larger samples of people; the same is true for the use of genomics in agriculture [57] and conservation genetics [55]. Recent work showed that evolutionary conservation accounts for the vast majority of the predictive power of a state-of-the-art deep learning approach to variant annotation [149, 150].…”

Section: Discussionmentioning

confidence: 99%

“…For example, in humans, evolutionary conserved sequences are enriched for trait and disease heritability [48, 49], and conservation across related species can be used to prioritize medically relevant variants in fine mapping [50, 51] and rare-variant association studies [52, 53]. Similarly, multi-species alignments are being used by conservation geneticists to estimate the fitness effects of mutations in wild populations [54, 55] and by plant breeders to aid in genomic selection [56, 57]. And there is growing interest in using estimated ancestral recombination graphs (ARGs) to perform explicitly tree-based versions of QTL mapping and complex trait analysis [58, 59].…”

Section: Introductionmentioning

confidence: 99%

Unifying approaches from statistical genetics and phylogenetics for mapping phenotypes in structured populations

Schraiber,

Edge,

Pennell

2024

Preprint

View full text Add to dashboard Cite

In both statistical genetics and phylogenetics, a major goal is to identify correlations between genetic loci or other aspects of the phenotype or environment and a focal trait. In these two fields, there are sophisticated but disparate statistical traditions aimed at these tasks. The disconnect between their respective approaches is becoming untenable as questions in medicine, conservation biology, and evolutionary biology increasingly rely on integrating data from within and among species and once clear conceptual divisions are becoming increasingly blurred. To help bridge this divide, we derive a general model describing the covariance between the genetic contributions to the quantitative phenotypes of different individuals. Taking this approach shows that standard models in both statistical genetics (e.g., Genome-Wide Association Studies; GWAS) and phylogenetic comparative biology (e.g., phylogenetic regression) can be interpreted as special cases of this more general quantitative-genetic model. The fact that these models share the same core architecture means that we can build a unified understanding of the strengths and limitations of different methods for controlling for genetic structure when testing for associations. We develop intuition for why and when spurious correlations may occur using analytical theory and conduct population genetic and phylogenetic simulations of quantitative traits to provide to a detailed analysis of the general regression model, in which both standard GWAS methods and phylogenetic regression are subsumed. This enables us to take methodological advances from one field and apply them in the other. We demonstrate this by showing how a standard GWAS technique---including both the genetic relatedness matrix (GRM) as well as its leading eigenvectors, corresponding the principal components (PCs) of the genotype matrix, in a regression model---can mitigate spurious correlations in phylogenetic analyses. As a case study of this, we re-examine an analysis testing for co-evolution of expression levels between genes across a fungal phylogeny, and show that including principal components as covariates decreases the false positive rate while simultaneously increasing the true positive rate. More generally, this work provides a foundation for more integrative approaches for understanding the genetic architecture of phenotypes and how evolutionary processes shape it.

show abstract

“…Potato (Solanum tuberosum) is an important food crop that is consumed by over a billion people each day (Devaux et al, 2021). Potato is an autopolyploid (2n = 4x = 48) that has a high degree of heterozygosity and numerous deleterious alleles in its genome (Spooner et al, 2014;Wu et al, 2023;Zhang et al, 2019). New potato varieties introduced over the past century have been identified using phenotypic selection of F1 populations.…”

Section: Introductionmentioning

confidence: 99%

A survey of the Sli gene in wild and cultivated potato

Ames,

Hamernik,

Behling

et al. 2024

Plant Direct

View full text Add to dashboard Cite

Inbred‐hybrid breeding of diploid potatoes necessitates breeding lines that are self‐compatible. One way of incorporating self‐compatibility into incompatible cultivated potato (Solanum tuberosum) germplasm is to introduce the S‐locus inhibitor gene (Sli), which functions as a dominant inhibitor of gametophytic self‐incompatibility. To learn more about Sli diversity and function in wild species relatives of cultivated potato, we obtained Sli gene sequences that extended from the 5′UTR to the 3′UTR from 133 individuals from 22 wild species relatives of potato and eight diverse cultivated potato clones. DNA sequence alignment and phylogenetic trees based on genomic and protein sequences show that there are two highly conserved groups of Sli sequences. DNA sequences in one group contain the 533 bp insertion upstream of the start codon identified previously in self‐compatible potato. The second group lacks the insertion. Three diploid and four polyploid individuals of wild species collected from geographically disjointed localities contained Sli with the 533 bp insertion. For most of the wild species clones examined, however, Sli did not have the insertion. Phylogenetic analysis indicated that Sli sequences with the insertion, in wild species and in cultivated clones, trace back to a single origin. Some diploid wild potatoes that have Sli with the insertion were self‐incompatible and some wild potatoes that lack the insertion were self‐compatible. Although there is evidence of positive selection for some codon positions in Sli, there is no evidence of diversifying selection at the gene level. In silico analysis of Sli protein structure did not support the hypothesis that amino acid changes from wild‐type (no insertion) to insertion‐type account for changes in protein function. Our study demonstrated that genetic factors besides the Sli gene must be important for conditioning a switch in the mating system from self‐incompatible to self‐compatible in wild potatoes.

show abstract

Phylogenomic discovery of deleterious mutations facilitates hybrid potato breeding

Cited by 19 publications

References 120 publications

Natural variation in potato sexual reproduction facilitates breeding

Natural variation in potato sexual reproduction facilitates breeding

Unifying approaches from statistical genetics and phylogenetics for mapping phenotypes in structured populations

A survey of the Sli gene in wild and cultivated potato

Contact Info

Product

Resources

About