Less Is More, Natural Loss-of-Function Mutation Is a Strategy for Adaptation

Xu, Yongchao; Guo, Ya‐Long

doi:10.1016/j.xplc.2020.100103

Cited by 40 publications

(29 citation statements)

References 97 publications

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“…These results suggest that mutigenerational growth of A. thaliana at high temperatures causes mutations in temperature response- or stress-associated genes. Given that mutations in some functional genes (e.g., loss-of-function) are important for plant adaptation [ 67 , 68 ], whether these gene mutations contribute to high-temperature adaptation of plants requires further investigation. We also found that one gene ( AT4G17760 ) associated with DNA repair and DNA damage checkpoints was mutated in a Heat MA line.…”

Section: Discussionmentioning

confidence: 99%

Genome-wide DNA mutations in Arabidopsis plants after multigenerational exposure to high temperatures

Cui

Wang

et al. 2021

Genome Biol

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Background Elevated temperatures can cause physiological, biochemical, and molecular responses in plants that can greatly affect their growth and development. Mutations are the most fundamental force driving biological evolution. However, how long-term elevations in temperature influence the accumulation of mutations in plants remains unknown. Results Multigenerational exposure of Arabidopsis MA (mutation accumulation) lines and MA populations to extreme heat and moderate warming results in significantly increased mutation rates in single-nucleotide variants (SNVs) and small indels. We observe distinctive mutational spectra under extreme and moderately elevated temperatures, with significant increases in transition and transversion frequencies. Mutation occurs more frequently in intergenic regions, coding regions, and transposable elements in plants grown under elevated temperatures. At elevated temperatures, more mutations accumulate in genes associated with defense responses, DNA repair, and signaling. Notably, the distribution patterns of mutations among all progeny differ between MA populations and MA lines, suggesting that stronger selection effects occurred in populations. Methylation is observed more frequently at mutation sites, indicating its contribution to the mutation process at elevated temperatures. Mutations occurring within the same genome under elevated temperatures are significantly biased toward low gene density regions, special trinucleotides, tandem repeats, and adjacent simple repeats. Additionally, mutations found in all progeny overlap significantly with genetic variations reported in 1001 Genomes, suggesting non-uniform distribution of de novo mutations through the genome. Conclusion Collectively, our results suggest that elevated temperatures can accelerate the accumulation, and alter the molecular profiles, of DNA mutations in plants, thus providing significant insight into how environmental temperatures fuel plant evolution.

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Section: Discussionmentioning

confidence: 99%

Genome-wide DNA mutations in Arabidopsis plants after multigenerational exposure to high temperatures

Cui

Wang

et al. 2021

Genome Biol

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“…It has been shown gene duplication and natural loss-offunction mutations change crop agronomic traits (Xu and Guo, 2020). Compared with A. thaliana, several core circadian clock genes of M. truncatula were found to be altered in copy number, and many of them were tissue-specific.…”

Section: Discussionmentioning

confidence: 99%

Circadian rhythms driving a fast‐paced root clock implicate species‐specific regulation in Medicago truncatula

Wang

Zhou

et al. 2021

JIPB

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Plants have a hierarchical circadian structure comprising multiple tissue-specific oscillators that operate at different speeds and regulate the expression of distinct sets of genes in different organs. However, the identity of the genes differentially regulated by the circadian clock in different organs, such as roots, and how their oscillations create functional specialization remain unclear. Here, we profiled the diurnal and circadian landscapes of the shoots and roots of Medicago truncatula and identified the conserved regulatory sequences contributing to transcriptome oscillations in each organ. We found that the light-dark cycles strongly affect the global transcriptome oscillation in roots, and many clock genes oscillate only in shoots. Moreover, many key genes involved in nitrogen fixation are regulated by circadian rhythms. Surprisingly, the root clock runs faster than the shoot clock, which is contrary to the hierarchical circadian structure showing a slow-paced root clock in both detached and intact Arabidopsis thaliana (L.) Heynh. roots. Our result provides important clues about the species-specific circadian regulatory mechanism, which is often overlooked, and possibly coordinates the timing between shoots and roots independent of the current prevailing model.

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“…The bloom of genomics is providing a new vision on gene loss as one of the major sources of genetic variation with great potential to contribute to evolutionary adaptation and the generation of biodiversity, and therefore to impact on the evolvability of groups of organisms ( Olson, 1999 ; Albalat and Cañestro, 2016 ; Sharma et al, 2018 ; Guijarro-Clarke et al, 2020 ; Helsen et al, 2020 ; Xu and Guo, 2020 ). Despite mutational events that lead to non-functionalization and gene loss are random, the analyses of biased patterns of gene loss can reveal relevant information about the evolutionary impact of the losses (reviewed in Albalat and Cañestro, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution

Martí-Solans

Godoy-Marín

Diaz-Gracia

et al. 2021

Front. Cell Dev. Biol.

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Gene loss is a pervasive source of genetic variation that influences species evolvability, biodiversity and the innovation of evolutionary adaptations. To better understand the evolutionary patterns and impact of gene loss, here we investigate as a case study the evolution of the wingless (Wnt) family in the appendicularian tunicate Oikopleura dioica, an emergent EvoDevo model characterized by its proneness to lose genes among chordates. Genome survey and phylogenetic analyses reveal that only four of the thirteen Wnt subfamilies have survived in O. dioica—Wnt5, Wnt10, Wnt11, and Wnt16,—representing the minimal Wnt repertoire described in chordates. While the loss of Wnt4 and Wnt8 likely occurred in the last common ancestor of tunicates, representing therefore a synapomorphy of this subphylum, the rest of losses occurred during the evolution of appendicularians. This work provides the first complete Wnt developmental expression atlas in a tunicate and the first insights into the evolution of Wnt developmental functions in appendicularians. Our work highlights three main evolutionary patterns of gene loss: (1) conservation of ancestral Wnt expression domains not affected by gene losses; (2) function shuffling among Wnt paralogs accompanied by gene losses; and (3) extinction of Wnt expression in certain embryonic directly correlated with gene losses. Overall our work reveals that in contrast to “conservative” pattern of evolution of cephalochordates and vertebrates, O. dioica shows an even more radical “liberal” evolutionary pattern than that described ascidian tunicates, stretching the boundaries of the malleability of Wnt family evolution in chordates.

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Less Is More, Natural Loss-of-Function Mutation Is a Strategy for Adaptation

Cited by 40 publications

References 97 publications

Genome-wide DNA mutations in Arabidopsis plants after multigenerational exposure to high temperatures

Genome-wide DNA mutations in Arabidopsis plants after multigenerational exposure to high temperatures

Circadian rhythms driving a fast‐paced root clock implicate species‐specific regulation in Medicago truncatula

Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution

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