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Title: Century-long timelines of herbarium genomes predict plant stomatal response to climate change

Journal Article · · Nature Ecology and Evolution

Abstract Dissecting plant responses to the environment is key to understanding whether and how plants adapt to anthropogenic climate change. Stomata, plants’ pores for gas exchange, are expected to decrease in density following increased CO 2 concentrations, a trend already observed in multiple plant species. However, it is unclear whether such responses are based on genetic changes and evolutionary adaptation. Here we make use of extensive knowledge of 43 genes in the stomatal development pathway and newly generated genome information of 191 Arabidopsis thaliana historical herbarium specimens collected over 193 years to directly link genetic variation with climate change. While we find that the essential transcription factors SPCH, MUTE and FAMA, central to stomatal development, are under strong evolutionary constraints, several regulators of stomatal development show signs of local adaptation in contemporary samples from different geographic regions. We then develop a functional score based on known effects of gene knock-out on stomatal development that recovers a classic pattern of stomatal density decrease over the past centuries, suggesting a genetic component contributing to this change. This approach combining historical genomics with functional experimental knowledge could allow further investigations of how different, even in historical samples unmeasurable, cellular plant phenotypes may have already responded to climate change through adaptive evolution.

Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0021286
OSTI ID:
2427423
Journal Information:
Nature Ecology and Evolution, Journal Name: Nature Ecology and Evolution Journal Issue: 9 Vol. 8; ISSN 2397-334X
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (95)

Isolation, Library Preparation, and Bioinformatic Analysis of Historical and Ancient Plant DNA journal November 2020
The arabidopsis information resource: Making and mining the “gold standard” annotated reference plant genome: Tair: Making and Mining the “Gold Standard” Plant Genome journal August 2015
Very high resolution interpolated climate surfaces for global land areas journal January 2005
Stomatal Density and Index of Fossil Plants Track Atmospheric Carbon Dioxide in the Palaeozoic journal October 1995
Evolutionary responses of stomatal density to global CO2 change journal April 1993
On the number of segregating sites in genetical models without recombination journal April 1975
BASL Controls Asymmetric Cell Division in Arabidopsis journal June 2009
1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana journal July 2016
The Signaling Peptide EPF2 Controls Asymmetric Cell Divisions during Stomatal Development journal May 2009
High temperature exposure increases plant cooling capacity journal May 2012
Direct Control of SPEECHLESS by PIF4 in the High-Temperature Response of Stomatal Development journal April 2018
MUTE Directly Orchestrates Cell-State Switch and the Single Symmetric Division to Create Stomata journal May 2018
Modulation of Asymmetric Division Diversity through Cytokinin and SPEECHLESS Regulatory Interactions in the Arabidopsis Stomatal Lineage journal October 2018
YODA-HSP90 Module Regulates Phosphorylation-Dependent Inactivation of SPEECHLESS to Control Stomatal Development under Acute Heat Stress in Arabidopsis journal April 2020
Stomata: key players in the earth system, past and present journal June 2010
Transcriptional control of cell fate in the stomatal lineage journal February 2016
Reinforcing plant evolutionary genomics using ancient DNA journal April 2017
Exploiting natural variation and genetic manipulation of stomatal conductance for crop improvement journal June 2019
Chemical control of stomatal function and development journal April 2021
Plasticity’s role in adaptive evolution depends on environmental change components journal December 2022
New Guidelines for δ 13 C Measurements journal April 2006
Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels journal June 1987
A globally coherent fingerprint of climate change impacts across natural systems journal January 2003
Termination of asymmetric cell division and differentiation of stomata journal December 2006
Transcription factor control of asymmetric cell divisions that establish the stomatal lineage journal December 2006
Stomagen positively regulates stomatal density in Arabidopsis journal December 2009
Genome-wide efficient mixed-model analysis for association studies journal June 2012
Fiji: an open-source platform for biological-image analysis journal June 2012
Precision genome engineering through adenine base editing in plants journal June 2018
Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana journal December 2017
Tutorial: a guide to performing polygenic risk score analyses journal July 2020
TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015 journal January 2018
Molecular control of stomatal development journal January 2018
African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana journal May 2017
Functional variants of DOG1 control seed chilling responses and variation in seasonal life-history strategies in Arabidopsis thaliana journal January 2020
Seasonal timing adaptation across the geographic range of Arabidopsis thaliana journal February 2020
Regional Differentiation in Plant Species journal May 1941
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses journal September 2007
Predicting Responses to Contemporary Environmental Change Using Evolutionary Response Architectures journal May 2017
Natural variation in stomatal abundance of Arabidopsis thaliana includes cryptic diversity for different developmental processes journal March 2011
The variant call format and VCFtools journal June 2011
mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters journal April 2013
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. journal November 1989
Twelve years of SAMtools and BCFtools journal January 2021
Was low CO2 a driving force of C4 evolution: Arabidopsis responses to long-term low CO2 stress journal May 2014
Epidermal Cell Density is Autoregulated via a Secretory Peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis Leaves journal May 2009
Temporal patterns of damage and decay kinetics of DNA retrieved from plant herbarium specimens journal June 2016
Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient journal February 2012
A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana journal May 2000
The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule journal July 2007
Illumina Sequencing Library Preparation for Highly Multiplexed Target Capture and Sequencing journal June 2010
Application of Optical Topometry to Analysis of the Plant Epidermis journal August 2015
Origins and Evolution of Stomatal Development journal March 2017
B1-Type Cyclin-Dependent Kinases Are Essential for the Formation of Stomatal Complexes in Arabidopsis thaliana journal March 2004
Arabidopsis FAMA Controls the Final Proliferation/Differentiation Switch during Stomatal Development journal October 2006
SCREAM/ICE1 and SCREAM2 Specify Three Cell-State Transitional Steps Leading to Arabidopsis Stomatal Differentiation journal July 2008
Manipulation of Mitogen-Activated Protein Kinase Kinase Signaling in the Arabidopsis Stomatal Lineage Reveals Motifs That Contribute to Protein Localization and Signaling Specificity   journal August 2014
A Repressor Protein Complex Regulates Leaf Growth in Arabidopsis journal July 2015
Hybridization ddRAD‐sequencing for population genomics of nonmodel plants using highly degraded historical specimen DNA journal May 2020
Contrasting responses of leaf stomatal characteristics to climate change: a considerable challenge to predict carbon and water cycles journal March 2017
Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana journal November 2019
Climate change and evolution: disentangling environmental and genetic responses journal January 2008
Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects?: Plant responses to high temperature and water deficit journal November 2011
Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools journal April 2016
Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana journal September 2018
Using herbaria to study global environmental change journal August 2018
Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO 2 journal October 2020
Control of Stomatal Distribution on the Arabidopsis Leaf Surface journal May 2002
Stomatal Development and Pattern Controlled by a MAPKK Kinase journal June 2004
Stomatal Patterning and Differentiation by Synergistic Interactions of Receptor Kinases journal July 2005
Paleoatmospheric Signatures in Neogene Fossil Leaves journal June 1993
Direct observation of adaptive tracking on ecological time scales in Drosophila journal March 2022
Ancient DNA genomics and the renaissance of herbaria journal October 2023
Ancient Plant Genomics in Archaeology, Herbaria, and the Environment journal April 2020
Ecological and Evolutionary Responses to Recent Climate Change journal December 2006
Stomatal Density as an Indicator of Atmospheric CO2 Concentration journal March 1992
A novel role for STOMATAL CARPENTER 1 in stomata patterning journal August 2016
EAGER: efficient ancient genome reconstruction journal March 2016
AdapterRemoval v2: rapid adapter trimming, identification, and read merging journal February 2016
Second-generation PLINK: rising to the challenge of larger and richer datasets journal February 2015
Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION 1 journal March 2014
The plant stomatal lineage at a glance journal April 2019
A spectrum of free software tools for processing the VCF variant call format: vcflib, bio-vcf, cyvcf2, hts-nim and slivar journal May 2022
A Population Genetic Signal of Polygenic Adaptation journal August 2014
The rate and potential relevance of new mutations in a colonizing plant lineage journal February 2018
Temporal Patterns of Nucleotide Misincorporations and DNA Fragmentation in Ancient DNA journal March 2012
Co-Variation between Seed Dormancy, Growth Rate and Flowering Time Changes with Latitude in Arabidopsis thaliana journal May 2013
Impact of Stomatal Density and Morphology on Water-Use Efficiency in a Changing World journal March 2019
Stomatal Lineage Control by Developmental Program and Environmental Cues journal October 2021
Herbarium specimens, photographs, and field observations show Philadelphia area plants are responding to climate change journal April 2012
Herbarium specimens demonstrate earlier flowering times in response to warming in Boston journal August 2004
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w journal April 2012
Historical Arabidopsis thaliana genomes from Germany dataset January 2022
Historical Arabidopsis thaliana genomes from across its native range. dataset January 2022
Supplementary Information for: Century-long timelines of herbarium genomes predict plant stomatal response to climate change text January 2024