Unstable Allotetraploid Tobacco Genome due to Frequent Homeologous Recombination, Segmental Deletion, and Chromosome Loss

Abstract

The types of mutations and their corresponding frequencies are difficult to measure in complex genomes. In this study, a high-throughput method was developed to identify spontaneous loss-of-function alleles for the resistance gene N and the transgenic avirulence gene P50 in allotetraploid tobacco. A total of 2134 loss-of-function alleles of the N gene were identified after screening 14 million F hybrids. Analysis of these mutants revealed striking evolutionary patterns for genes in polyploids. Only 14 of the loss-of-function mutations were caused by spontaneous point mutations or indels, while the others were caused by homeologous recombination (with a frequency of ∼1/12 000) or chromosome loss (∼1/15 000). Loss of the chromosome with the P50 insertion occurred at a similar frequency (∼1/13 000), and the frequency of spontaneous segmental deletion in this chromosome was ∼1/16 000. Both homeologous recombination and chromosome loss considerably decreased the viability of the mutants. Our data suggest that the high mutation rate in polyploids is probably due to the occurrence of homeologous recombination and the tolerance of large mutations such as chromosome loss in polyploid genomes. Frequent mutations tend to drive polyploids to extinction unless a novel mutation helps the polyploid to effectively compete with diploids or find a new ecological niche.

Homoeologous Exchanges, Segmental Allopolyploidy, and Polyploid Genome Evolution

“…Homoeologous exchanges are now known to be common in synthetic polyploids, as well as those of recent evolutionary origin. Recent allopolyploids with commonly detected HEs include Tragopogon species ( Chester et al, 2012 ), peanuts ( Arachis hypogaea ; Bertioli et al, 2019 ; Zhuang et al, 2019 ), quinoa ( Chenopodium quinoa ; Jarvis et al, 2017 ), tobacco ( Nicotiana tabacum ; Chen et al, 2018 ) and rapeseed ( Brassica napus ; Chalhoub et al, 2014 ). Synthetics with frequent HEs include allopolyploid rice (constructed from Oryza sativa subsp.…”

Genomics of Evolutionary Novelty in Hybrids and Polyploids

“…Classically recognized as homoeologous translocations or transpositions, the genomics era and the successful sequencing of polyploid plants ushered in an increasing realization that HEs represent a fundamental mechanism of allopolyploid genome evolution and for generating diversity. Recent illustrative examples include peanuts ( Arachis hypogaea ; Bertioli et al, 2019 ; Zhuang et al, 2019 ), Tragopogon ( Chester et al, 2012 ), quinoa ( Chenopodium quinoa ; Jarvis et al, 2017 ), Brassica ( Hurgobin et al, 2018 ; Samans et al, 2018 ), tobacco ( Nicotiana tabacum ; Chen et al, 2018 ) and allopolyploid rice (constructed from Oryza sativa subsp. indica × subsp.…”

Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

“…Repeated allopolyploid formation or gene flow from diploids (e.g., Brachypodium hybridum - [122], Arabidopsis suecica - [174]) can cause N e to differ across subgenomes. Finally, recombination could also act to bias inferences of ω artifactually because genetic material exchanged across subgenomes via homoeologous exchange [18][19][20][21][22][23][24][25][175][176][177][178][179][180][181][182][183], gene conversion [19,20,57,62,133,153,[184][185][186][187][188][189], and other recombinational mechanisms (e.g., [190]) would be expected to bias ω inferred across a topologically constrained tree. However, we took steps to prevent this type of artifact from influencing our data by only including genes that exhibited gene-tree topologies that were consistent with the species tree topology.…”

“…Accordingly, evolutionary biologists have had a great deal of interest in exploring the consequences of and responses to WGD. The ensuing studies have shown that the effects of WGDs are far-ranging, including silencing and loss of duplicated genes [5][6][7][8][9][10][11], mobilization of previously dormant transposable elements [12][13][14][15][16][17], inter-genomic gene conversion and homoeologous chromosome exchanges [18][19][20][21][22][23][24][25], alterations of epigenetic marks [26][27][28][29][30][31][32][33], massive, genome-wide transcriptional rewiring [6,[34][35][36][37][38][39][40][41], and a host of other associated physiological, ecological, and life-history changes [42][43][44][45][46][47][48][49]…”