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Probing the response of the amphibious plant Butomus umbellatus to nutrient enrichment and shading by integrating eco-physiological with metabolomic analyses

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Probing the response of the amphibious plant Butomus umbellatus to nutrient enrichment and shading by integrating eco-physiological with metabolomic analyses. / Manolaki, Paraskevi; Tooulakou, Georgia ; Byberg, Caroline Urup; Eller, Franziska; Sorrell, Brian Keith; Klapa, Maria I.; Riis, Tenna.

In: Frontiers in Plant Science, Vol. 11, 581787, 12.2020.

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@article{52297d549a424b6c98cbba9258f39975,
title = "Probing the response of the amphibious plant Butomus umbellatus to nutrient enrichment and shading by integrating eco-physiological with metabolomic analyses",
abstract = "Amphibious plants, living in land-water ecotones, have to cope with challenging and continuously changing growth conditions in their habitats with respect to nutrient and light availability. They have thus evolved a variety of mechanisms to tolerate and adapt to these changes. Therefore, the study of these plants is a major area of ecophysiology and environmental ecological research. However, our understanding of their capacity for physiological adaptation and tolerance remains limited and requires systemic approaches for comprehensive analyses. To this end, in this study, we have conducted a mesocosm experiment to analyze the response of Butomus umbellatus, a common amphibious species in Denmark, to nutrient enrichment and shading. Our study follows a systematic integration of morphological (including plant height, leaf number, and biomass accumulation), ecophysiological (photosynthesis-irradiance responses, leaf pigment content, and C and N content in plant organs), and leaf metabolomic measurements using gas chromatography-mass spectrometry (39 mainly primary metabolites), based on bioinformatic methods. No studies of this type have been previously reported for this plant species. We observed that B. umbellatus responds to nutrient enrichment and light reduction through different mechanisms and were able to identify its nutrient enrichment acclimation threshold within the applied nutrient gradient. Up to that threshold, the morpho-physiological response to nutrient enrichment was profound, indicating fast-growing trends (higher growth rates and biomass accumulation), but only few parameters changed significantly from light to shade [specific leaf area (SLA); quantum yield (φ)]. Metabolomic analysis supported the morpho-physiological results regarding nutrient overloading, indicating also subtle changes due to shading not directly apparent in the other measurements. The combined profile analysis revealed leaf metabolite and morpho-physiological parameter associations. In this context, leaf lactate, currently of uncertain role in higher plants, emerged as a shading acclimation biomarker, along with SLA and φ. The study enhances both the ecophysiology methodological toolbox and our knowledge of the adaptive capacity of amphibious species. It demonstrates that the educated combination of physiological with metabolomic measurements using bioinformatic approaches is a promising approach for ecophysiology research, enabling the elucidation of discriminatory metabolic shifts to be used for early diagnosis and even prognosis of natural ecosystem responses to climate change.",
keywords = "Butomus umbellatus, abiotic plant stresses, amphibious plants, eco-metabolomics, ecophysiology, nutrient enrichment, shading effect, systems biology",
author = "Paraskevi Manolaki and Georgia Tooulakou and Byberg, {Caroline Urup} and Franziska Eller and Sorrell, {Brian Keith} and Klapa, {Maria I.} and Tenna Riis",
year = "2020",
month = dec,
doi = "10.3389/fpls.2020.581787",
language = "English",
volume = "11",
journal = "Frontiers in Plant Science",
issn = "1664-462X",
publisher = "Frontiers Media S.A",

}

RIS

TY - JOUR

T1 - Probing the response of the amphibious plant Butomus umbellatus to nutrient enrichment and shading by integrating eco-physiological with metabolomic analyses

AU - Manolaki, Paraskevi

AU - Tooulakou, Georgia

AU - Byberg, Caroline Urup

AU - Eller, Franziska

AU - Sorrell, Brian Keith

AU - Klapa, Maria I.

AU - Riis, Tenna

PY - 2020/12

Y1 - 2020/12

N2 - Amphibious plants, living in land-water ecotones, have to cope with challenging and continuously changing growth conditions in their habitats with respect to nutrient and light availability. They have thus evolved a variety of mechanisms to tolerate and adapt to these changes. Therefore, the study of these plants is a major area of ecophysiology and environmental ecological research. However, our understanding of their capacity for physiological adaptation and tolerance remains limited and requires systemic approaches for comprehensive analyses. To this end, in this study, we have conducted a mesocosm experiment to analyze the response of Butomus umbellatus, a common amphibious species in Denmark, to nutrient enrichment and shading. Our study follows a systematic integration of morphological (including plant height, leaf number, and biomass accumulation), ecophysiological (photosynthesis-irradiance responses, leaf pigment content, and C and N content in plant organs), and leaf metabolomic measurements using gas chromatography-mass spectrometry (39 mainly primary metabolites), based on bioinformatic methods. No studies of this type have been previously reported for this plant species. We observed that B. umbellatus responds to nutrient enrichment and light reduction through different mechanisms and were able to identify its nutrient enrichment acclimation threshold within the applied nutrient gradient. Up to that threshold, the morpho-physiological response to nutrient enrichment was profound, indicating fast-growing trends (higher growth rates and biomass accumulation), but only few parameters changed significantly from light to shade [specific leaf area (SLA); quantum yield (φ)]. Metabolomic analysis supported the morpho-physiological results regarding nutrient overloading, indicating also subtle changes due to shading not directly apparent in the other measurements. The combined profile analysis revealed leaf metabolite and morpho-physiological parameter associations. In this context, leaf lactate, currently of uncertain role in higher plants, emerged as a shading acclimation biomarker, along with SLA and φ. The study enhances both the ecophysiology methodological toolbox and our knowledge of the adaptive capacity of amphibious species. It demonstrates that the educated combination of physiological with metabolomic measurements using bioinformatic approaches is a promising approach for ecophysiology research, enabling the elucidation of discriminatory metabolic shifts to be used for early diagnosis and even prognosis of natural ecosystem responses to climate change.

AB - Amphibious plants, living in land-water ecotones, have to cope with challenging and continuously changing growth conditions in their habitats with respect to nutrient and light availability. They have thus evolved a variety of mechanisms to tolerate and adapt to these changes. Therefore, the study of these plants is a major area of ecophysiology and environmental ecological research. However, our understanding of their capacity for physiological adaptation and tolerance remains limited and requires systemic approaches for comprehensive analyses. To this end, in this study, we have conducted a mesocosm experiment to analyze the response of Butomus umbellatus, a common amphibious species in Denmark, to nutrient enrichment and shading. Our study follows a systematic integration of morphological (including plant height, leaf number, and biomass accumulation), ecophysiological (photosynthesis-irradiance responses, leaf pigment content, and C and N content in plant organs), and leaf metabolomic measurements using gas chromatography-mass spectrometry (39 mainly primary metabolites), based on bioinformatic methods. No studies of this type have been previously reported for this plant species. We observed that B. umbellatus responds to nutrient enrichment and light reduction through different mechanisms and were able to identify its nutrient enrichment acclimation threshold within the applied nutrient gradient. Up to that threshold, the morpho-physiological response to nutrient enrichment was profound, indicating fast-growing trends (higher growth rates and biomass accumulation), but only few parameters changed significantly from light to shade [specific leaf area (SLA); quantum yield (φ)]. Metabolomic analysis supported the morpho-physiological results regarding nutrient overloading, indicating also subtle changes due to shading not directly apparent in the other measurements. The combined profile analysis revealed leaf metabolite and morpho-physiological parameter associations. In this context, leaf lactate, currently of uncertain role in higher plants, emerged as a shading acclimation biomarker, along with SLA and φ. The study enhances both the ecophysiology methodological toolbox and our knowledge of the adaptive capacity of amphibious species. It demonstrates that the educated combination of physiological with metabolomic measurements using bioinformatic approaches is a promising approach for ecophysiology research, enabling the elucidation of discriminatory metabolic shifts to be used for early diagnosis and even prognosis of natural ecosystem responses to climate change.

KW - Butomus umbellatus

KW - abiotic plant stresses

KW - amphibious plants

KW - eco-metabolomics

KW - ecophysiology

KW - nutrient enrichment

KW - shading effect

KW - systems biology

UR - http://www.scopus.com/inward/record.url?scp=85098480069&partnerID=8YFLogxK

U2 - 10.3389/fpls.2020.581787

DO - 10.3389/fpls.2020.581787

M3 - Journal article

C2 - 33391296

VL - 11

JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

SN - 1664-462X

M1 - 581787

ER -