In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction

Volatile organic compounds (VOCs) comprises a broad class of small molecules (up to ~300 g/mol) produced by biological and non-biological sources. VOCs play a vital role in an organism’s metabolism during its growth, defense, and reproduction. The well-known 6-pentyl-<inline-formula><math x...

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Main Authors: Rosina Torres-Ortega, Héctor Guillén-Alonso, Raúl Alcalde-Vázquez, Enrique Ramírez-Chávez, Jorge Molina-Torres, Robert Winkler
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Metabolites
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Online Access:https://www.mdpi.com/2218-1989/12/12/1231
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author Rosina Torres-Ortega
Héctor Guillén-Alonso
Raúl Alcalde-Vázquez
Enrique Ramírez-Chávez
Jorge Molina-Torres
Robert Winkler
author_facet Rosina Torres-Ortega
Héctor Guillén-Alonso
Raúl Alcalde-Vázquez
Enrique Ramírez-Chávez
Jorge Molina-Torres
Robert Winkler
author_sort Rosina Torres-Ortega
collection DOAJ
description Volatile organic compounds (VOCs) comprises a broad class of small molecules (up to ~300 g/mol) produced by biological and non-biological sources. VOCs play a vital role in an organism’s metabolism during its growth, defense, and reproduction. The well-known 6-pentyl-<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mi>α</mi></semantics></math></inline-formula>-pyrone (6-PP) molecule is an example of a major volatile biosynthesized by <i>Trichoderma atroviride</i> that modulates the expression of PIN auxin-transport proteins in primary roots of <i>Arabidopsis thaliana</i> during their relationship. Their beneficial relation includes lateral root formation, defense induction, and increased plant biomass production. The role of 6-PP has been widely studied due to its relevance in this cross-kingdom relationship. Conventional VOCs measurements are often destructive; samples require further preparation, and the time resolution is low (around hours). Some techniques enable at-line or real-time analyses but are highly selective to defined compounds. Due to these technical constraints, it is difficult to acquire relevant information about the dynamics of VOCs in biological systems. Low-temperature plasma (LTP) ionization allows the analysis of a wide range of VOCs by mass spectrometry (MS). In addition, LTP-MS requires no sample preparation, is solvent-free, and enables the detection of 6-PP faster than conventional analytical methods. Applying static statistical methods such as Principal Component Analysis (PCA) and Discriminant Factorial Analysis (DFA) leads to a loss of information since the biological systems are dynamic. Thus, we applied a time series analysis to find patterns in the signal changes. Our results indicate that the 6-PP signal is constitutively emitted by <i>T. atroviride</i> only; the signal shows high skewness and kurtosis. In <i>A. thaliana</i> grown alone, no signal corresponding to 6-PP is detected above the white noise level. However, during <i>T. atroviride-A. thaliana</i> interaction, the signal performance showed reduced skewness and kurtosis with high autocorrelation. These results suggest that 6-PP is a physiological variable that promotes homeostasis during the plant-fungal relationship. Although the molecular mechanism of this cross-kingdom control is still unknown, our study indicates that 6-PP has to be regulated by <i>A. thaliana</i> during their interaction.
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spelling doaj.art-99d6dfd9bf7d499aa778ec1b3bdd77dc2023-11-24T16:37:57ZengMDPI AGMetabolites2218-19892022-12-011212123110.3390/metabo12121231In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal InteractionRosina Torres-Ortega0Héctor Guillén-Alonso1Raúl Alcalde-Vázquez2Enrique Ramírez-Chávez3Jorge Molina-Torres4Robert Winkler5Department of Biotechnology and Biochemistry, Center for Research and Advanced Studies (CINVESTAV), Irapuato 36824, MexicoDepartment of Biotechnology and Biochemistry, Center for Research and Advanced Studies (CINVESTAV), Irapuato 36824, MexicoDepartment of Biotechnology and Biochemistry, Center for Research and Advanced Studies (CINVESTAV), Irapuato 36824, MexicoDepartment of Biotechnology and Biochemistry, Center for Research and Advanced Studies (CINVESTAV), Irapuato 36824, MexicoDepartment of Biotechnology and Biochemistry, Center for Research and Advanced Studies (CINVESTAV), Irapuato 36824, MexicoDepartment of Biotechnology and Biochemistry, Center for Research and Advanced Studies (CINVESTAV), Irapuato 36824, MexicoVolatile organic compounds (VOCs) comprises a broad class of small molecules (up to ~300 g/mol) produced by biological and non-biological sources. VOCs play a vital role in an organism’s metabolism during its growth, defense, and reproduction. The well-known 6-pentyl-<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><mi>α</mi></semantics></math></inline-formula>-pyrone (6-PP) molecule is an example of a major volatile biosynthesized by <i>Trichoderma atroviride</i> that modulates the expression of PIN auxin-transport proteins in primary roots of <i>Arabidopsis thaliana</i> during their relationship. Their beneficial relation includes lateral root formation, defense induction, and increased plant biomass production. The role of 6-PP has been widely studied due to its relevance in this cross-kingdom relationship. Conventional VOCs measurements are often destructive; samples require further preparation, and the time resolution is low (around hours). Some techniques enable at-line or real-time analyses but are highly selective to defined compounds. Due to these technical constraints, it is difficult to acquire relevant information about the dynamics of VOCs in biological systems. Low-temperature plasma (LTP) ionization allows the analysis of a wide range of VOCs by mass spectrometry (MS). In addition, LTP-MS requires no sample preparation, is solvent-free, and enables the detection of 6-PP faster than conventional analytical methods. Applying static statistical methods such as Principal Component Analysis (PCA) and Discriminant Factorial Analysis (DFA) leads to a loss of information since the biological systems are dynamic. Thus, we applied a time series analysis to find patterns in the signal changes. Our results indicate that the 6-PP signal is constitutively emitted by <i>T. atroviride</i> only; the signal shows high skewness and kurtosis. In <i>A. thaliana</i> grown alone, no signal corresponding to 6-PP is detected above the white noise level. However, during <i>T. atroviride-A. thaliana</i> interaction, the signal performance showed reduced skewness and kurtosis with high autocorrelation. These results suggest that 6-PP is a physiological variable that promotes homeostasis during the plant-fungal relationship. Although the molecular mechanism of this cross-kingdom control is still unknown, our study indicates that 6-PP has to be regulated by <i>A. thaliana</i> during their interaction.https://www.mdpi.com/2218-1989/12/12/1231AIMS LTP-MSkurtosisVOCs monitoringtime series in VOCs emissions
spellingShingle Rosina Torres-Ortega
Héctor Guillén-Alonso
Raúl Alcalde-Vázquez
Enrique Ramírez-Chávez
Jorge Molina-Torres
Robert Winkler
In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction
Metabolites
AIMS LTP-MS
kurtosis
VOCs monitoring
time series in VOCs emissions
title In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction
title_full In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction
title_fullStr In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction
title_full_unstemmed In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction
title_short In Vivo Low-Temperature Plasma Ionization Mass Spectrometry (LTP-MS) Reveals Regulation of 6-Pentyl-2H-Pyran-2-One (6-PP) as a Physiological Variable during Plant-Fungal Interaction
title_sort in vivo low temperature plasma ionization mass spectrometry ltp ms reveals regulation of 6 pentyl 2h pyran 2 one 6 pp as a physiological variable during plant fungal interaction
topic AIMS LTP-MS
kurtosis
VOCs monitoring
time series in VOCs emissions
url https://www.mdpi.com/2218-1989/12/12/1231
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