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

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. Further, 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) inmore » 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.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [2]; ORCiD logo [2]; ORCiD logo [3];  [4]; ORCiD logo [2];  [2];  [2];  [2];  [5];  [1];  [6];  [7];  [8] more »; ORCiD logo [8];  [9];  [10];  [8];  [11]; ORCiD logo [1]; ORCiD logo [2] « less
  1. New York Univ. (NYU), NY (United States)
  2. Fondo de Desarrollo de Areas Prioritarias (FONDAP) Center for Genome Regulation, Santiago (Chile); Pontifica Universidad Catolica de Chile, Santiago (Chile)
  3. Purdue Univ., West Lafayette, IN (United States)
  4. American Museum of Natural History (AMNH), New York, NY (United States); Academia Sinica, Taipei (Taiwan)
  5. Fondo de Desarrollo de Areas Prioritarias (FONDAP) Center for Genome Regulation, Santiago (Chile); Pontifica Universidad Catolica de Chile, Santiago (Chile); Universidad Mayor, Santiago (Chile)
  6. Fondo de Desarrollo de Areas Prioritarias (FONDAP) Center for Genome Regulation, Santiago (Chile); Universidad Andres Bello, Santiago (Chile)
  7. Fondo de Desarrollo de Areas Prioritarias (FONDAP) Center for Genome Regulation, Santiago (Chile); Universidad Andres Bello, Santiago (Chile)
  8. Fondo de Desarrollo de Areas Prioritarias (FONDAP) Center for Genome Regulation, Santiago (Chile); Universidad de Chile, Santiago (Chile)
  9. American Museum of Natural History (AMNH), New York, NY (United States)
  10. New York Botanical Garden, Bronx, NY (United States)
  11. Pontifica Universidad Catolica de Chile, Santiago (Chile)
Publication Date:
Research Org.:
New York Univ. (NYU), NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1832144
Grant/Contract Number:  
SC0014377
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 118; Journal Issue: 46; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; desert; evolution; adaptation; stress; microbiome; genomics

Citation Formats

Eshel, Gil, Araus, Viviana, Undurraga, Soledad, Soto, Daniela C., Moraga, Carol, Montecinos, Alejandro, Moyano, Tomás, Maldonado, Jonathan, Díaz, Francisca P., Varala, Kranthi, Nelson, Chase W., Contreras-López, Orlando, Pal-Gabor, Henrietta, Kraiser, Tatiana, Carrasco-Puga, Gabriela, Nilo-Poyanco, Ricardo, Zegar, Charles M., Orellana, Ariel, Montecino, Martín, Maass, Alejandro, Allende, Miguel L., DeSalle, Robert, Stevenson, Dennis W., González, Mauricio, Latorre, Claudio, Coruzzi, Gloria M., and Gutiérrez, Rodrigo A.. Plant ecological genomics at the limits of life in the Atacama Desert. United States: N. p., 2021. Web. doi:10.1073/pnas.2101177118.
Eshel, Gil, Araus, Viviana, Undurraga, Soledad, Soto, Daniela C., Moraga, Carol, Montecinos, Alejandro, Moyano, Tomás, Maldonado, Jonathan, Díaz, Francisca P., Varala, Kranthi, Nelson, Chase W., Contreras-López, Orlando, Pal-Gabor, Henrietta, Kraiser, Tatiana, Carrasco-Puga, Gabriela, Nilo-Poyanco, Ricardo, Zegar, Charles M., Orellana, Ariel, Montecino, Martín, Maass, Alejandro, Allende, Miguel L., DeSalle, Robert, Stevenson, Dennis W., González, Mauricio, Latorre, Claudio, Coruzzi, Gloria M., & Gutiérrez, Rodrigo A.. Plant ecological genomics at the limits of life in the Atacama Desert. United States. https://doi.org/10.1073/pnas.2101177118
Eshel, Gil, Araus, Viviana, Undurraga, Soledad, Soto, Daniela C., Moraga, Carol, Montecinos, Alejandro, Moyano, Tomás, Maldonado, Jonathan, Díaz, Francisca P., Varala, Kranthi, Nelson, Chase W., Contreras-López, Orlando, Pal-Gabor, Henrietta, Kraiser, Tatiana, Carrasco-Puga, Gabriela, Nilo-Poyanco, Ricardo, Zegar, Charles M., Orellana, Ariel, Montecino, Martín, Maass, Alejandro, Allende, Miguel L., DeSalle, Robert, Stevenson, Dennis W., González, Mauricio, Latorre, Claudio, Coruzzi, Gloria M., and Gutiérrez, Rodrigo A.. Mon . "Plant ecological genomics at the limits of life in the Atacama Desert". United States. https://doi.org/10.1073/pnas.2101177118. https://www.osti.gov/servlets/purl/1832144.
@article{osti_1832144,
title = {Plant ecological genomics at the limits of life in the Atacama Desert},
author = {Eshel, Gil and Araus, Viviana and Undurraga, Soledad and Soto, Daniela C. and Moraga, Carol and Montecinos, Alejandro and Moyano, Tomás and Maldonado, Jonathan and Díaz, Francisca P. and Varala, Kranthi and Nelson, Chase W. and Contreras-López, Orlando and Pal-Gabor, Henrietta and Kraiser, Tatiana and Carrasco-Puga, Gabriela and Nilo-Poyanco, Ricardo and Zegar, Charles M. and Orellana, Ariel and Montecino, Martín and Maass, Alejandro and Allende, Miguel L. and DeSalle, Robert and Stevenson, Dennis W. and González, Mauricio and Latorre, Claudio and Coruzzi, Gloria M. and Gutiérrez, Rodrigo A.},
abstractNote = {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. Further, 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.},
doi = {10.1073/pnas.2101177118},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 46,
volume = 118,
place = {United States},
year = {2021},
month = {11}
}

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