Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function

Abstract

Interdisciplinary syntheses are needed to scale up discovery of the environmental drivers and molecular basis of adaptation in nature. Here we integrated novel approaches using whole genome sequences, satellite remote sensing, and transgenic experiments to study natural loss-of-function alleles associated with drought histories in wild Arabidopsis thaliana. The genes we identified exhibit population genetic signatures of parallel molecular evolution, selection for loss-of-function, and shared associations with flowering time phenotypes in directions consistent with longstanding adaptive hypotheses seven times more often than expected by chance. We then confirmed predicted phenotypes experimentally in transgenic knockout lines. These findings reveal the importance of drought timing to explain the evolution of alternative drought tolerance strategies and further challenge popular assumptions about the adaptive value of genetic loss-of-function in nature. These results also motivate improved species-wide sequencing efforts to better identify loss-of-function variants and inspire new opportunities for engineering climate resilience in crops.

In the presence of population structure: From genomics to candidate genes underlying local adaptation

“…Given the significant enrichment of such SNPs among low‐frequency‐derived alleles that show poor direct and indirect evidence of local adaptation, we raise caution when interpreting such results. Enrichment of climate‐associated SNPs along nonsynonymous sites (Hancock, Brachi, et al, ; Hancock, Witonsky, et al, ; Lasky et al, ) or the parallel occurrence of low‐frequency loss‐of‐function mutations showing significant associations with climate (Monroe et al, , ) has been interpreted as evidence of adaptation. Although such signals may represent instances of adaptation, they can also be explained by neutral evolution, in which relaxed selection across specific climates results in the enrichment of independent loss‐of‐function mutations or nonsynonymous variation (Flowers, Hanzawa, Hall, Moore, & Purugganan, ; Zhen, Dhakal, & Ungerer, ; Zhen & Ungerer, ).…”

“…As a study system, we use the species Arabidopsis thaliana, hereafter mentioned as Arabidopsis. Arabidopsis populations are found all across Eurasia (1001Genomes Consortium, 2016, traversing very different climates (Frachon et al, 2018;Lasky et al, 2012;Mojica et al, 2016;Monroe et al, 2018), and therefore have been thought to be locally adapted. Direct evidence of local adaptation has been observed between North Sweden and Central Italy populations (Ågren & Schemske, 2012;Fournier-Level et al, 2011), in which the fitness of genotypes was measured in a reciprocal transplant experiment at the native sites of each population (Ågren & Schemske, 2012); and recombinant inbred lines of these were used to map quantitative trait loci (QTL) explaining fitness variation (Ågren et al, 2013).…”

Allelic Variation in the Chloroplast Division Gene FtsZ2-2 Leads to Natural Variation in Chloroplast Size

“…While large-effect QTLs are often associated with allelic variation in regulatory regions that impact gene expression (Maloof et al, 2001;Bartlett and Whipple, 2013), our data show that variation in the FtsZ2-2 coding sequence influences chloroplast size through multiple protein-based mechanisms. Similarly, polymorphisms producing various truncated and other predicted loss-of-function proteins or altering single amino acids have been shown to be important determinants of several life-history and whole-plant traits, including flowering time, flower color and pollinator preference, drought tolerance, trichome patterning, and photomorphogenesis (Le Corre et al, 2002;Shindo et al, 2005;Balasubramanian et al, 2006;Hoballah et al, 2007;Monroe et al, 2018). In these cases, the relatively high frequency of such mutations suggests that they may confer a selective advantage.…”

Transcriptional natural variation at FLM induces synergistic pleiotropy in Arabidopsis thaliana

“…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).…”