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Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness

Plants respond to environmental cues via adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This Umwelt underlies steady dynamics, due to complex local and global biotic and abiotic changes...

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Autores principales: Bharadwaj, Revuru, Noceda, Carlos, Mohanapriya, Gunasekharan, Kumar, Sarma Rajeev, Thiers, Karine Leitão Lima, Costa, José Hélio, Macedo, Elisete Santos, Kumari, Aprajita, Gupta, Kapuganti Jagadis, Srivastava, Shivani, Adholeya, Alok, Oliveira, Manuela, Velada, Isabel, Sircar, Debabrata, Sathishkumar, Ramalingam, Arnholdt-Schmitt, Birgit
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518632/
https://www.ncbi.nlm.nih.gov/pubmed/34659277
http://dx.doi.org/10.3389/fpls.2021.686274
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author Bharadwaj, Revuru
Noceda, Carlos
Mohanapriya, Gunasekharan
Kumar, Sarma Rajeev
Thiers, Karine Leitão Lima
Costa, José Hélio
Macedo, Elisete Santos
Kumari, Aprajita
Gupta, Kapuganti Jagadis
Srivastava, Shivani
Adholeya, Alok
Oliveira, Manuela
Velada, Isabel
Sircar, Debabrata
Sathishkumar, Ramalingam
Arnholdt-Schmitt, Birgit
author_facet Bharadwaj, Revuru
Noceda, Carlos
Mohanapriya, Gunasekharan
Kumar, Sarma Rajeev
Thiers, Karine Leitão Lima
Costa, José Hélio
Macedo, Elisete Santos
Kumari, Aprajita
Gupta, Kapuganti Jagadis
Srivastava, Shivani
Adholeya, Alok
Oliveira, Manuela
Velada, Isabel
Sircar, Debabrata
Sathishkumar, Ramalingam
Arnholdt-Schmitt, Birgit
author_sort Bharadwaj, Revuru
collection PubMed
description Plants respond to environmental cues via adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This Umwelt underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, adaptive plant holobiont responses are crucial for continuous metabolic adjustment at the systems level. Plants require oxygen-dependent respiration for energy-dependent adaptive morphology, such as germination, root and shoot growth, and formation of adventitious, clonal, and reproductive organs, fruits, and seeds. Fermentative paths can help in acclimation and, to our view, the role of alternative oxidase (AOX) in coordinating complex metabolic and physiological adjustments is underestimated. Cellular levels of sucrose are an important sensor of environmental stress. We explored the role of exogenous sucrose and its interplay with AOX during early seed germination. We found that sucrose-dependent initiation of fermentation during the first 12 h after imbibition (HAI) was beneficial to germination. However, parallel upregulated AOX expression was essential to control negative effects by prolonged sucrose treatment. Early downregulated AOX activity until 12 HAI improved germination efficiency in the absence of sucrose but suppressed early germination in its presence. The results also suggest that seeds inoculated with arbuscular mycorrhizal fungi (AMF) can buffer sucrose stress during germination to restore normal respiration more efficiently. Following this approach, we propose a simple method to identify organic seeds and low-cost on-farm perspectives for early identifying disease tolerance, predicting plant holobiont behavior, and improving germination. Furthermore, the research strengthens the view that AOX can serve as a powerful functional marker source for seed hologenomes.
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spelling pubmed-85186322021-10-16 Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness Bharadwaj, Revuru Noceda, Carlos Mohanapriya, Gunasekharan Kumar, Sarma Rajeev Thiers, Karine Leitão Lima Costa, José Hélio Macedo, Elisete Santos Kumari, Aprajita Gupta, Kapuganti Jagadis Srivastava, Shivani Adholeya, Alok Oliveira, Manuela Velada, Isabel Sircar, Debabrata Sathishkumar, Ramalingam Arnholdt-Schmitt, Birgit Front Plant Sci Plant Science Plants respond to environmental cues via adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This Umwelt underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, adaptive plant holobiont responses are crucial for continuous metabolic adjustment at the systems level. Plants require oxygen-dependent respiration for energy-dependent adaptive morphology, such as germination, root and shoot growth, and formation of adventitious, clonal, and reproductive organs, fruits, and seeds. Fermentative paths can help in acclimation and, to our view, the role of alternative oxidase (AOX) in coordinating complex metabolic and physiological adjustments is underestimated. Cellular levels of sucrose are an important sensor of environmental stress. We explored the role of exogenous sucrose and its interplay with AOX during early seed germination. We found that sucrose-dependent initiation of fermentation during the first 12 h after imbibition (HAI) was beneficial to germination. However, parallel upregulated AOX expression was essential to control negative effects by prolonged sucrose treatment. Early downregulated AOX activity until 12 HAI improved germination efficiency in the absence of sucrose but suppressed early germination in its presence. The results also suggest that seeds inoculated with arbuscular mycorrhizal fungi (AMF) can buffer sucrose stress during germination to restore normal respiration more efficiently. Following this approach, we propose a simple method to identify organic seeds and low-cost on-farm perspectives for early identifying disease tolerance, predicting plant holobiont behavior, and improving germination. Furthermore, the research strengthens the view that AOX can serve as a powerful functional marker source for seed hologenomes. Frontiers Media S.A. 2021-10-01 /pmc/articles/PMC8518632/ /pubmed/34659277 http://dx.doi.org/10.3389/fpls.2021.686274 Text en Copyright © 2021 Bharadwaj, Noceda, Mohanapriya, Kumar, Thiers, Costa, Macedo, Kumari, Gupta, Srivastava, Adholeya, Oliveira, Velada, Sircar, Sathishkumar and Arnholdt-Schmitt. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Bharadwaj, Revuru
Noceda, Carlos
Mohanapriya, Gunasekharan
Kumar, Sarma Rajeev
Thiers, Karine Leitão Lima
Costa, José Hélio
Macedo, Elisete Santos
Kumari, Aprajita
Gupta, Kapuganti Jagadis
Srivastava, Shivani
Adholeya, Alok
Oliveira, Manuela
Velada, Isabel
Sircar, Debabrata
Sathishkumar, Ramalingam
Arnholdt-Schmitt, Birgit
Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
title Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
title_full Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
title_fullStr Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
title_full_unstemmed Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
title_short Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
title_sort adaptive reprogramming during early seed germination requires temporarily enhanced fermentation-a critical role for alternative oxidase regulation that concerns also microbiota effectiveness
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518632/
https://www.ncbi.nlm.nih.gov/pubmed/34659277
http://dx.doi.org/10.3389/fpls.2021.686274
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