Adaptation and Phenotypic Diversification in Arabidopsis through Loss-of-Function Mutations in Protein-Coding Genes

Xu, Yongchao; Niu, Xiao‐Min; Li, Xinxin; He, Wenrong; Chen, Jiafu; Zou, Yu-Pan; Wu, Qiong; Zhang, Yong E.; Busch, Wolfgang; Guo, Ya‐Long

doi:10.1105/tpc.18.00791

Cited by 44 publications

(59 citation statements)

References 76 publications

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“…SnpEff predicted 4,163 premature stop codons, 3,238 lost stop codons, and 8,065 frameshifts based on this variant set (File S5). Even given the larger genome size, these numbers are substantially higher than high impact variant numbers observed in re-sequencing studies of homozygous species before (Pucker et al 2016;Xu et al 2019). One explanation could be the presence of three alleles for each locus leading to compensation of disrupted alleles.…”

Section: Genome-wide Distribution Of Small Sequence Variantsmentioning

confidence: 91%

Genome Sequencing of Musa acuminata Dwarf Cavendish Reveals a Duplication of a Large Segment of Chromosome 2

Busche¹,

Pucker²,

Viehöver³

et al. 2020

G3 Genes|Genomes|Genetics

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Different Musa species, subspecies, and cultivars are currently investigated to reveal their genomic diversity. Here, we compare the genome sequence of one of the commercially most important cultivars, Musa acuminata Dwarf Cavendish, against the Pahang reference genome assembly. Numerous small sequence variants were detected and the ploidy of the cultivar presented here was determined as triploid based on sequence variant frequencies. Illumina sequence data also revealed a duplication of a large segment on the long arm of chromosome 2 in the Dwarf Cavendish genome. Comparison against previously sequenced cultivars provided evidence that this duplication is unique to Dwarf Cavendish. Although no functional relevance of this duplication was identified, this example shows the potential of plants to tolerate such aneuploidies.

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Section: Genome-wide Distribution Of Small Sequence Variantsmentioning

confidence: 91%

Genome Sequencing of Musa acuminata Dwarf Cavendish Reveals a Duplication of a Large Segment of Chromosome 2

Busche¹,

Pucker²,

Viehöver³

et al. 2020

G3 Genes|Genomes|Genetics

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“…Having an FLM knock-down (by the substitution SNP28958) instead of a knock-out would allow to keep a certain thermosensitivity while coordinately shifting several other traits important for leaf growth. Loss-of-function mutations were proposed to play a substantial role in plant adaptation (Monroe et al, 2018;Xu et al, 2019). However, the selective value of such natural mutations was rarely demonstrated so far (Poormohammad Kiani et al, 2012;Gujas et al, 2012;Wu et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Transcriptional natural variation at FLM induces synergistic pleiotropy in Arabidopsis thaliana

Hanemian

Vasseur

Marchadier

et al. 2019

Preprint

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Investigating the evolution of complex phenotypes and the underlying molecular bases of their variation is critical to understand how organisms adapt to the environment. We used leaf growth as a model trait as it is highly integrative of internal and external cues and relies on functions at different levels of the plant organization. Applying classical quantitative genetics on a recombinant inbred line population derived from a Can-0 x Col-0 cross, we identified the MADSbox transcription factor FLOWERING LOCUS M (FLM) as a player of the phenotypic variation for leaf growth and colour. Interestingly, we showed that allelic variation at FLM modulates plant growth strategy along the leaf economics spectrum, a trade-off between resource acquisition and resource conservation observable across thousands of plant species. We demonstrated that the functional differences at FLM relies on a single intronic substitution, disturbing transcript splicing and leading to a low expression of the active FLM transcript. Using phenotypic and climatic data across Arabidopsis natural populations, our work shows how noncoding genetic variation of a single gene may be adaptive through synergistic pleiotropy.

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“…Indeed, loss-of-function mutations occur widely in laboratory evolution experiments [5,8,[13][14][15][16], suggesting this is a common mode of adaptation to a new environment. However, few experiments have tested how such lost functions could be restored.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary regain of lost gene circuit function

Gouda

Manhart

Balazsi³

2019

Preprint

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Evolutionary reversibility -the ability to regain a lost function -is an important problem both in evolutionary and synthetic biology, where repairing natural or synthetic systems broken by evolutionary processes may be valuable. Here, we use a synthetic positivefeedback (PF) gene circuit integrated into haploid Saccharomyces cerevisiae cells to test if the population can restore lost PF function. In previous evolution experiments, mutations in a gene eliminated the fitness costs of PF activation. Since PF activation also provides drug resistance, exposing such compromised or broken mutants to both drug and inducer should create selection pressure to regain drug resistance and possibly PF function. Indeed, evolving seven PF mutant strains in the presence of drug revealed three adaptation scenarios through genomic mutations outside of the PF circuit that elevate PF basal expression, possibly by affecting transcription, translation, degradation and other fundamental cell functions. Nonfunctional mutants gained drug resistance without ever developing high expression, while quasi-functional and dysfunctional PF mutants developed high expression which then diminished, although more slowly for dysfunctional mutants where revertant clones arose. These results highlight how intracellular context, such as the growth rate, can affect regulatory network dynamics and evolutionary dynamics, which has important consequences for understanding the evolution of drug resistance and developing future synthetic biology applications. Significance Statement Natural or synthetic genetic modules can lose their function over long-term evolution if the function is costly. How populations can evolve to restore broken functions is poorly understood. To test the reversibility of evolutionary breakdown, we use yeast cell populations with a chromosomally integrated synthetic gene circuit. In previous evolution experiments the gene circuit lost its costly function through various mutations. By exposing such mutant populations to conditions where regaining gene circuit function would be beneficial we find adaptation scenarios with or without repairing lost gene circuit function. These results are important for drug resistance or future synthetic biology applications where loss and regain of function play a significant role.

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Adaptation and Phenotypic Diversification in Arabidopsis through Loss-of-Function Mutations in Protein-Coding Genes

Cited by 44 publications

References 76 publications

Genome Sequencing of Musa acuminata Dwarf Cavendish Reveals a Duplication of a Large Segment of Chromosome 2

Genome Sequencing of Musa acuminata Dwarf Cavendish Reveals a Duplication of a Large Segment of Chromosome 2

Transcriptional natural variation at FLM induces synergistic pleiotropy in Arabidopsis thaliana

Evolutionary regain of lost gene circuit function

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