No abstract

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.

The search for novel stress tolerance determinants has led to increasing interest in plants native to extreme environments – so called “extremophytes.” One successful strategy has been comparative studies between Arabidopsis thaliana and extremophyte Brassicaceae relatives such as the halophyte Eutrema salsugineum located in areas including cold, salty coastal regions of China. Here, we investigate stress tolerance in the desert species, Anastatica hierochuntica (True Rose of Jericho), a member of the poorly investigated lineage III Brassicaceae. We show that A. hierochuntica has a genome approximately 4.5-fold larger than Arabidopsis, divided into 22 diploid chromosomes, and demonstrate that A. hierochuntica exhibits tolerance to heat, low N and salt stresses that are characteristic of its habitat. Taking salt tolerance as a case study, we show that A. hierochuntica shares common salt tolerance mechanisms with E. salsugineum such as tight control of shoot Na+ accumulation and resilient photochemistry features. Furthermore, metabolic profiling of E. salsugineum and A. hierochuntica shoots demonstrates that the extremophytes exhibit both species-specific and common metabolic strategies to cope with salt stress including constitutive up-regulation (under control and salt stress conditions) of ascorbate and dehydroascorbate, two metabolites involved in ROS scavenging. Accordingly, A. hierochuntica displays tolerance to methyl viologen-induced oxidative stress suggesting that a highly active antioxidant system is essential to cope with multiple abiotic stresses. We suggest that A. hierochuntica presents an excellent extremophyte Arabidopsis relative model system for understanding plant survival in harsh desert conditions.

Placozoa is an ancient phylum of extraordinarily unusual animals: miniscule, ameboid creatures that lack most fundamental animal features. Despite high genetic diversity, only recently have the second and third species been named. While prior genomic studies suffer from incomplete placozoan taxon sampling, we more than double the count with protein sequences from seven key genomes and produce the first nuclear phylogenomic reconstruction of all major placozoan lineages. This leads us to the first complete Linnaean taxonomic classification of Placozoa, over a century after its discovery: This may be the only time in the 21st century when an entire higher taxonomy for a whole animal phylum is formalized. Our classification establishes 2 new classes, 4 new orders, 3 new families, 1 new genus, and 1 new species, namely classes Polyplacotomia and Uniplacotomia; orders Polyplacotomea, Trichoplacea, Cladhexea, and Hoilungea; families Polyplacotomidae, Cladtertiidae, and Hoilungidae; and genus Cladtertia with species Cladtertia collaboinventa, nov. Our likelihood and gene content tree topologies refine the relationships determined in previous studies. Adding morphological data into our phylogenomic matrices suggests sponges (Porifera) as the sister to other animals, indicating that modest data addition shifts this node away from comb jellies (Ctenophora). Furthermore, by adding the first genomic protein data of the exceptionally distinct and branching Polyplacotoma mediterranea, we solidify its position as sister to all other placozoans; a divergence we estimate to be over 400 million years old. Yet even this deep split sits on a long branch to other animals, suggesting a bottleneck event followed by diversification. Ancestral state reconstructions indicate large shifts in gene content within Placozoa, with Hoilungia hongkongensis and its closest relatives having the most unique genetics.

Non-photochemical quenching (NPQ) plays a major role in photoprotection. Anastatica hierochuntica is an annual desert plant found in hot deserts. We compared A. hierochuntica to three other different species: Arabidopsis thaliana, Eutrema salsugineum and Helianthus annuus, which have different NPQ and photosynthetic capacities. Anastatica hierochuntica plants had very different induction kinetics of NPQ and, to a lesser extent, of photosystem II electron transport rate (PSII ETR), in comparison to all other plants species in the experiments. The major components of the unusual photosynthetic and photoprotective response in A. hierochuntica were: (1) Low NPQ at the beginning of the light period, at various light intensities and CO2 concentrations. The described low NPQ cannot be explained by low leaf absorbance or by low energy distribution to PSII, but was related to the de-epoxidation state of xanthophylls. (2) Relatively high PSII ETR at various CO2 concentrations in correlation with low NPQ. PSII ETR responded positively to the increase of CO2 concentrations. At low CO2 concentrations PSII ETR was mostly O2 dependent. At moderate and high CO2 concentrations the high PSII ETR in A. hierochuntica was accompanied by relatively high CO2 assimilation rates. We suggest that A. hierochuntica have an uncommon NPQ and PSII ETR response. These responses in A. hierochuntica might represent an adaptation to the short growing season of an annual desert plant.