Evidence from the proteome for local adaptation to extreme heat in a widespread tree species

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Heatwaves are increasing in frequency and intensity globally with negative consequences for biological function. Assessing the effect of extreme heat on species requires an understanding of their adaptive capacity for mitigating physiological damage. Where long-term exposure to extreme heat in natural populations provides sufficient selection pressure, populations should exhibit signals of adaptive thermotolerance to temperature extremes.

Using quantitative proteomics, we tested this idea in the widespread and commercially important tree species Eucalyptus grandis (Flooded Gum). Seedlings from six natural populations of E. grandis spanning a 2,000 km gradient were exposed to a four-day extreme heat treatment (42–24°C day–night cycle) in experimental growth chambers. Populations differed in their long-term exposure to extreme heat conditions, defined both as the number of days annually ≥15°C above mean annual temperature (MAT), and average number of days annually with temperature maxima ≥35°C between 1960 and 1990.

Long-term exposure to extreme heat conditions in the field predicted the protein-level response of E. grandis to experimental heatwaves. Relationships between long-term extreme heat exposure and protein increases were positive and linear for all combinations of extreme heat (days ≥15°C above MAT, mean days with temperature maxima ≥35°C annually) and expression (all differentially expressed proteins, isolated heat shock proteins, proteins involved in molecular stress responses).

Although extreme climate events are typically rare (e.g., 1 day 15° ≥MAT per 5 years in some populations in our study), E. grandis populations sampled from across a 2,000 km range exhibit a clear capacity to increase expression of proteins involved in heat stress in response to simulated heatwave exposure. Presumably, they respond similarly under natural heatwave conditions.

We show that a long-lived species with a broad environmental niche exhibits adaptive variation in protein response to temperature extremes at the population level. This implies that restoration, translocation and silvicultural programmes should consider the molecular response of source populations to climatic extremes to maximize success under future climates. Tree populations with low exposure to extreme heat conditions may be limited in their ability to respond to heatwave events, potentially limiting their adaptive capacity to withstand novel climate conditions.

LanguageEnglish
Pages436-446
Number of pages11
JournalFunctional Ecology
Volume33
Issue number3
Early online date9 Dec 2018
DOIs
Publication statusPublished - Mar 2019

Fingerprint

local adaptation
proteome
heat
protein
Eucalyptus grandis
temperature
chronic exposure
climate
proteins
population pressure
proteomics
heat shock
climate conditions
translocation
exposure
niche
heat tolerance
growth chambers
heat shock proteins
heat wave

Keywords

  • adaptive capacity
  • climate change
  • Eucalyptus grandis
  • extreme climates
  • extreme events
  • heatwaves
  • shotgun proteomics
  • thermal tolerance

Cite this

@article{69ed8af5d80e4416814765ef6921548c,
title = "Evidence from the proteome for local adaptation to extreme heat in a widespread tree species",
abstract = "Heatwaves are increasing in frequency and intensity globally with negative consequences for biological function. Assessing the effect of extreme heat on species requires an understanding of their adaptive capacity for mitigating physiological damage. Where long-term exposure to extreme heat in natural populations provides sufficient selection pressure, populations should exhibit signals of adaptive thermotolerance to temperature extremes.Using quantitative proteomics, we tested this idea in the widespread and commercially important tree species Eucalyptus grandis (Flooded Gum). Seedlings from six natural populations of E. grandis spanning a 2,000 km gradient were exposed to a four-day extreme heat treatment (42–24°C day–night cycle) in experimental growth chambers. Populations differed in their long-term exposure to extreme heat conditions, defined both as the number of days annually ≥15°C above mean annual temperature (MAT), and average number of days annually with temperature maxima ≥35°C between 1960 and 1990.Long-term exposure to extreme heat conditions in the field predicted the protein-level response of E. grandis to experimental heatwaves. Relationships between long-term extreme heat exposure and protein increases were positive and linear for all combinations of extreme heat (days ≥15°C above MAT, mean days with temperature maxima ≥35°C annually) and expression (all differentially expressed proteins, isolated heat shock proteins, proteins involved in molecular stress responses).Although extreme climate events are typically rare (e.g., 1 day 15° ≥MAT per 5 years in some populations in our study), E. grandis populations sampled from across a 2,000 km range exhibit a clear capacity to increase expression of proteins involved in heat stress in response to simulated heatwave exposure. Presumably, they respond similarly under natural heatwave conditions.We show that a long-lived species with a broad environmental niche exhibits adaptive variation in protein response to temperature extremes at the population level. This implies that restoration, translocation and silvicultural programmes should consider the molecular response of source populations to climatic extremes to maximize success under future climates. Tree populations with low exposure to extreme heat conditions may be limited in their ability to respond to heatwave events, potentially limiting their adaptive capacity to withstand novel climate conditions.",
keywords = "adaptive capacity, climate change, Eucalyptus grandis, extreme climates, extreme events, heatwaves, shotgun proteomics, thermal tolerance",
author = "Timothy Maher and Mehdi Mirzaei and Dana Pascovici and Wright, {Ian J.} and Haynes, {Paul A.} and Gallagher, {Rachael V.}",
year = "2019",
month = "3",
doi = "10.1111/1365-2435.13260",
language = "English",
volume = "33",
pages = "436--446",
journal = "Functional Ecology",
issn = "0269-8463",
publisher = "Wiley-Blackwell, Wiley",
number = "3",

}

Evidence from the proteome for local adaptation to extreme heat in a widespread tree species. / Maher, Timothy; Mirzaei, Mehdi; Pascovici, Dana; Wright, Ian J.; Haynes, Paul A.; Gallagher, Rachael V.

In: Functional Ecology, Vol. 33, No. 3, 03.2019, p. 436-446.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Evidence from the proteome for local adaptation to extreme heat in a widespread tree species

AU - Maher,Timothy

AU - Mirzaei,Mehdi

AU - Pascovici,Dana

AU - Wright,Ian J.

AU - Haynes,Paul A.

AU - Gallagher,Rachael V.

PY - 2019/3

Y1 - 2019/3

N2 - Heatwaves are increasing in frequency and intensity globally with negative consequences for biological function. Assessing the effect of extreme heat on species requires an understanding of their adaptive capacity for mitigating physiological damage. Where long-term exposure to extreme heat in natural populations provides sufficient selection pressure, populations should exhibit signals of adaptive thermotolerance to temperature extremes.Using quantitative proteomics, we tested this idea in the widespread and commercially important tree species Eucalyptus grandis (Flooded Gum). Seedlings from six natural populations of E. grandis spanning a 2,000 km gradient were exposed to a four-day extreme heat treatment (42–24°C day–night cycle) in experimental growth chambers. Populations differed in their long-term exposure to extreme heat conditions, defined both as the number of days annually ≥15°C above mean annual temperature (MAT), and average number of days annually with temperature maxima ≥35°C between 1960 and 1990.Long-term exposure to extreme heat conditions in the field predicted the protein-level response of E. grandis to experimental heatwaves. Relationships between long-term extreme heat exposure and protein increases were positive and linear for all combinations of extreme heat (days ≥15°C above MAT, mean days with temperature maxima ≥35°C annually) and expression (all differentially expressed proteins, isolated heat shock proteins, proteins involved in molecular stress responses).Although extreme climate events are typically rare (e.g., 1 day 15° ≥MAT per 5 years in some populations in our study), E. grandis populations sampled from across a 2,000 km range exhibit a clear capacity to increase expression of proteins involved in heat stress in response to simulated heatwave exposure. Presumably, they respond similarly under natural heatwave conditions.We show that a long-lived species with a broad environmental niche exhibits adaptive variation in protein response to temperature extremes at the population level. This implies that restoration, translocation and silvicultural programmes should consider the molecular response of source populations to climatic extremes to maximize success under future climates. Tree populations with low exposure to extreme heat conditions may be limited in their ability to respond to heatwave events, potentially limiting their adaptive capacity to withstand novel climate conditions.

AB - Heatwaves are increasing in frequency and intensity globally with negative consequences for biological function. Assessing the effect of extreme heat on species requires an understanding of their adaptive capacity for mitigating physiological damage. Where long-term exposure to extreme heat in natural populations provides sufficient selection pressure, populations should exhibit signals of adaptive thermotolerance to temperature extremes.Using quantitative proteomics, we tested this idea in the widespread and commercially important tree species Eucalyptus grandis (Flooded Gum). Seedlings from six natural populations of E. grandis spanning a 2,000 km gradient were exposed to a four-day extreme heat treatment (42–24°C day–night cycle) in experimental growth chambers. Populations differed in their long-term exposure to extreme heat conditions, defined both as the number of days annually ≥15°C above mean annual temperature (MAT), and average number of days annually with temperature maxima ≥35°C between 1960 and 1990.Long-term exposure to extreme heat conditions in the field predicted the protein-level response of E. grandis to experimental heatwaves. Relationships between long-term extreme heat exposure and protein increases were positive and linear for all combinations of extreme heat (days ≥15°C above MAT, mean days with temperature maxima ≥35°C annually) and expression (all differentially expressed proteins, isolated heat shock proteins, proteins involved in molecular stress responses).Although extreme climate events are typically rare (e.g., 1 day 15° ≥MAT per 5 years in some populations in our study), E. grandis populations sampled from across a 2,000 km range exhibit a clear capacity to increase expression of proteins involved in heat stress in response to simulated heatwave exposure. Presumably, they respond similarly under natural heatwave conditions.We show that a long-lived species with a broad environmental niche exhibits adaptive variation in protein response to temperature extremes at the population level. This implies that restoration, translocation and silvicultural programmes should consider the molecular response of source populations to climatic extremes to maximize success under future climates. Tree populations with low exposure to extreme heat conditions may be limited in their ability to respond to heatwave events, potentially limiting their adaptive capacity to withstand novel climate conditions.

KW - adaptive capacity

KW - climate change

KW - Eucalyptus grandis

KW - extreme climates

KW - extreme events

KW - heatwaves

KW - shotgun proteomics

KW - thermal tolerance

UR - http://www.scopus.com/inward/record.url?scp=85060570268&partnerID=8YFLogxK

UR - http://purl.org/au-research/grants/arc/DE170100208

UR - http://purl.org/au-research/grants/arc/FT100100910

U2 - 10.1111/1365-2435.13260

DO - 10.1111/1365-2435.13260

M3 - Article

VL - 33

SP - 436

EP - 446

JO - Functional Ecology

T2 - Functional Ecology

JF - Functional Ecology

SN - 0269-8463

IS - 3

ER -