Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation

Marylaure De La Harpe; Margot Paris; Jaqueline Hess; Michael Harald Johannes Barfuss; Martha Liliana Serrano-Serrano; Arindam Ghatak; Palak Chaturvedi; Wolfram Weckwerth; Walter Till; Nicolas Salamin; Ching Man Wai; Ray Ming; Christian Lexer

doi:10.1111/pce.13847

Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation

Marylaure De La Harpe, Margot Paris^*, Jaqueline Hess, Michael Harald Johannes Barfuss, Martha Liliana Serrano-Serrano, Arindam Ghatak, Palak Chaturvedi, Wolfram Weckwerth, Walter Till, Nicolas Salamin, Ching Man Wai, Ray Ming, Christian Lexer

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

15 Scopus citations

Abstract

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or “key innovations” including the transition from C₃ to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches, complemented by differential gene expression (RNA-seq) and targeted metabolite profiling, to address the mechanisms of C₃/CAM evolution in the extremely species-rich bromeliad genus, Tillandsia, and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C₃/CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar- and light-dependent regulation of growth and development. Our analyses also support the re-programming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation.

Original language	English (US)
Pages (from-to)	2987-3001
Number of pages	15
Journal	Plant Cell and Environment
Volume	43
Issue number	12
DOIs	https://doi.org/10.1111/pce.13847
State	Published - Dec 2020

Funding

We thank Michael Kessler and other members and collaborators of Swiss SNSF Sinergia project CRSII3_147630 for helpful discussions; Emiliano Trucchi for preliminary analyses of the data and helpful discussions, the SNSF for funding; Talita Machado for some accession sampling; staff of all living collections and service facilities used; the Next Generation Sequencing Platform in Bern for Illumina sequencing; and Jim Leebens-Mack and Karolina Heyduk for commenting on earlier versions of the paper.

Keywords

Bromeliaceae
adaptive radiation
circadian period length
copy number variation
drought
genome
transcriptome

ASJC Scopus subject areas

Physiology
Plant Science

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10.1111/pce.13847

Cite this

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title = "Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation",

abstract = "The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or “key innovations” including the transition from C3 to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches, complemented by differential gene expression (RNA-seq) and targeted metabolite profiling, to address the mechanisms of C3/CAM evolution in the extremely species-rich bromeliad genus, Tillandsia, and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C3/CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar- and light-dependent regulation of growth and development. Our analyses also support the re-programming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation.",

keywords = "Bromeliaceae, adaptive radiation, circadian period length, copy number variation, drought, genome, transcriptome",

author = "{De La Harpe}, Marylaure and Margot Paris and Jaqueline Hess and Barfuss, {Michael Harald Johannes} and Serrano-Serrano, {Martha Liliana} and Arindam Ghatak and Palak Chaturvedi and Wolfram Weckwerth and Walter Till and Nicolas Salamin and Wai, {Ching Man} and Ray Ming and Christian Lexer",

note = "Funding Information: We thank Michael Kessler and other members and collaborators of Swiss SNSF Sinergia project CRSII3_147630 for helpful discussions; Emiliano Trucchi for preliminary analyses of the data and helpful discussions, the SNSF for funding; Talita Machado for some accession sampling; staff of all living collections and service facilities used; the Next Generation Sequencing Platform in Bern for Illumina sequencing; and Jim Leebens-Mack and Karolina Heyduk for commenting on earlier versions of the paper. Publisher Copyright: {\textcopyright} 2020 John Wiley & Sons Ltd",

year = "2020",

month = dec,

doi = "10.1111/pce.13847",

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volume = "43",

pages = "2987--3001",

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AU - De La Harpe, Marylaure

AU - Paris, Margot

AU - Hess, Jaqueline

AU - Barfuss, Michael Harald Johannes

AU - Serrano-Serrano, Martha Liliana

AU - Ghatak, Arindam

AU - Chaturvedi, Palak

AU - Weckwerth, Wolfram

AU - Till, Walter

AU - Salamin, Nicolas

AU - Wai, Ching Man

AU - Ming, Ray

AU - Lexer, Christian

N1 - Funding Information: We thank Michael Kessler and other members and collaborators of Swiss SNSF Sinergia project CRSII3_147630 for helpful discussions; Emiliano Trucchi for preliminary analyses of the data and helpful discussions, the SNSF for funding; Talita Machado for some accession sampling; staff of all living collections and service facilities used; the Next Generation Sequencing Platform in Bern for Illumina sequencing; and Jim Leebens-Mack and Karolina Heyduk for commenting on earlier versions of the paper. Publisher Copyright: © 2020 John Wiley & Sons Ltd

PY - 2020/12

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N2 - The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by shifts in several adaptive traits or “key innovations” including the transition from C3 to CAM photosynthesis associated with xeric (heat/drought) adaptation. We used phylogenomic approaches, complemented by differential gene expression (RNA-seq) and targeted metabolite profiling, to address the mechanisms of C3/CAM evolution in the extremely species-rich bromeliad genus, Tillandsia, and related taxa. Evolutionary analyses of whole-genome sequencing and RNA-seq data suggest that evolution of CAM is associated with coincident changes to different pathways mediating xeric adaptation in this group. At the molecular level, C3/CAM shifts were accompanied by gene expansion of XAP5 CIRCADIAN TIMEKEEPER homologs, a regulator involved in sugar- and light-dependent regulation of growth and development. Our analyses also support the re-programming of abscisic acid-related gene expression via differential expression of ABF2/ABF3 transcription factor homologs, and adaptive sequence evolution of an ENO2/LOS2 enolase homolog, effectively tying carbohydrate flux to abscisic acid-mediated abiotic stress response. By pinpointing different regulators of overlapping molecular responses, our results suggest plausible mechanistic explanations for the repeated evolution of correlated adaptive traits seen in a textbook example of an adaptive radiation.

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KW - drought

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KW - transcriptome

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Genomic footprints of repeated evolution of CAM photosynthesis in a Neotropical species radiation

Abstract

Funding

Keywords

ASJC Scopus subject areas

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