The Atacama Desert in Chile—hyperarid and with high–ultraviolet irradiance levels—is one of the harshest environments on Earth. Yet, dozens of species grow there, including Atacama-endemic plants. Herein, we establish the Talabre–Lejía transect (TLT) in the Atacama as an unparalleled natural laboratory to study plant adaptation to extreme environmental conditions. We characterized climate, soil, plant, and soil–microbe diversity at 22 sites (every 100 m of altitude) along the TLT over a 10-y period. We quantified drought, nutrient deficiencies, large diurnal temperature oscillations, and pH gradients that define three distinct vegetational belts along the altitudinal cline. We deep-sequenced transcriptomes of 32 dominant plant species spanning the major plant clades, and assessed soil microbes by metabarcoding sequencing. The top-expressed genes in the 32 Atacama species are enriched in stress responses, metabolism, and energy production. Moreover, their root-associated soils are enriched in growth-promoting bacteria, including nitrogen fixers. To identify genes associated with plant adaptation to harsh environments, we compared 32 Atacama species with the 32 closest sequenced species, comprising 70 taxa and 1,686,950 proteins. To perform phylogenomic reconstruction, we concatenated 15,972 ortholog groups into a supermatrix of 8,599,764 amino acids. Using two codon-based methods, we identified 265 candidate positively selected genes (PSGs) in the Atacama plants, 64% of which are located in Pfam domains, supporting their functional relevance. For 59/184 PSGs with an Arabidopsis ortholog, we uncovered functional evidence linking them to plant resilience. As some Atacama plants are closely related to staple crops, these candidate PSGs are a “genetic goldmine” to engineer crop resilience to face climate change.

Comprehending ecological dynamics requires not only knowledge of modern communities but also detailed reconstructions of ecosystem history. Ancient DNA (aDNA) metabarcoding allows biodiversity responses to major climatic change to be explored at different spatial and temporal scales. We extracted aDNA preserved in fossil rodent middens to reconstruct late Quaternary vegetation dynamics in the hyperarid Atacama Desert. By comparing our paleo‐informed millennial record with contemporary observations of interannual variations in diversity, we show local plant communities behave differentially at different timescales. In the interannual (years to decades) time frame, only annual herbaceous expand and contract their distributional ranges (emerging from persistent seed banks) in response to precipitation, whereas perennials distribution appears to be extraordinarily resilient. In contrast, at longer timescales (thousands of years) many perennial species were displaced up to 1,000 m downslope during pluvial events. Given ongoing and future natural and anthropogenically induced climate change, our results not only provide baselines for vegetation in the Atacama Desert, but also help to inform how these and other high mountain plant communities may respond to fluctuations of climate in the future.

Estimating total plant diversity in extreme or hyperarid environments can be challenging, as adaptations to pronounced climate variability include evading prolonged stress periods through seeds or specialized underground organs. Short-term surveys of these ecosystems are thus likely poor estimators of actual diversity. Here we develop a multimethod strategy to obtain a more complete understanding of plant diversity from a community in the Atacama Desert. We explicitly test environmental DNA-based techniques (eDNA) to see if they can reveal the observed and 'hidden' (dormant or locally rare) species. To estimate total plant diversity, we performed long-term traditional surveys during eight consecutive years, including El Niño and La Niña events, we then analyzed eDNA from soil samples using high-throughput sequencing. We further used soil pollen analysis and soil seed bank germination assays to identify 'hidden' species. Each approach offers different subsets of current biodiversity at different taxonomic, spatial and temporal resolution, with a total of 92 taxa identified along the transect. Traditional field surveys identified 77 plant species over eight consecutive years. Observed community composition greatly varies interannually, with only 22 species seen every year. eDNA analysis revealed 37 taxa, eight of which were 'hidden' in our field surveys. Soil samples contain a viable seed bank of 21 taxa. Soil pollen (27 taxa) and eDNA analysis show affinities with vegetation at the landscape scale but a weak relationship to local plot diversity. Multimethod approaches (including eDNA) in deserts are valuable tools that add to a comprehensive assessment of biodiversity in such extreme environments, where using a single method or observations over a few years is insufficient. Our results can also explain the resilience of Atacama plant communities as 'hidden' taxa may have been active in the recent past or could even emerge in the future as accelerated global environmental change continues unabated.

A critical barrier to improving crop yield is the trade-off between seed weight (SW) and seed number (SN), which has been commonly reported in several crops, including Brassica napus. Despite the agronomic relevance of this issue, the molecular factors involved in the interaction between SW and SN are largely unknown in crops. In this work, we performed a detailed transcriptomic analysis of 48 seed samples obtained from two rapeseed spring genotypes subjected to different source–sink (S–S) ratios in order to examine the relationship between SW and SN under different field conditions. A multifactorial analysis of the RNA-seq data was used to identify a group of 1014 genes exclusively regulated by the S–S ratio. We found that a reduction in the S–S ratio during seed filling induces the expression of genes involved in sucrose transport, seed weight, and stress responses. Moreover, we identified five co-expression modules that are positively correlated with SW and negatively correlated with SN. Interestingly, one of these modules was significantly enriched in transcription factors (TFs). Furthermore, our network analysis predicted several NAC TFs as major hubs underlying SW and SN compensation. Taken together, our study provides novel insights into the molecular factors associated with the SW–SN relationship in rapeseed and identifies TFs as potential targets when improving crop yield.