Plant ecological genomics at the limits of life in the Atacama Desert

Gil Eshel, Viviana Araus, Soledad Undurraga, Daniela C. Soto, Carol Moraga, Alejandro Montecinos, Tomas Moyano, Jonathan Maldonado, Francisca P. iaz, Kranthi Varala, Chase W. Nelson, Orlando Contreras-Lopez, Henrietta Pal-Gabor, Tatiana Kraiser, Gabriela Carrasco-Puga, Ricardo Nilo-Poyanco, Charles M. Zegar, Ariel Orellana, Martin Montecino, Alejandro MaassMiguel L. Allende, Robert DeSalle, Dennis W. Stevenson, Mauricio Gonzalez, Claudio Latorre, Gloria M. Coruzzi*, Rodrigo A. Gutierrez*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

39 Scopus citations

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-Lejia 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 growthpromoting 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 codonbased 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.

Original languageEnglish
Article numbere2101177118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number46
DOIs
StatePublished - 16 Nov 2021
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Keywords

  • Adaptation
  • Desert
  • Evolution
  • Microbiome
  • Stress

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