Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
Autor(a) principal: | |
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Data de Publicação: | 2021 |
Outros Autores: | , , , , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/10174/32899 https://doi.org/10.3389/fpls.2021.686274 |
Resumo: | 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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Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectivenessseed qualityROSWarburg effectbacterial endophytes and mycorrhizal fungiorganic seedsbiotic stresson-farm seed selectionPlants 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.RS, GM, and BA-S acknowledge support for academic cooperation and mobility of researchers by the India-Portugal Bilateral Cooperation Program (2013–2015), funded by “Fundação para a Ciência e Tecnologia” (FCT), Portugal, and the Department of Science and Technology (DST), India. RS lab is financially supported by UGC-SAP and DST-FIST. GM was grateful to UGC, India, for a doctoral grant from the BSR fellowship. KG, MO, and BA-S acknowledge support by the India-Portugal Bilateral Cooperation Program “DST/INT/Portugal/P-03/2017.” MO research was partially supported by National Funds through FCT, Fundação para a Ciência e a Tecnologia projects UIDB/04674/2020 (CIMA). BA-S wants to thank RS for enabling intensive external online supervision of RB on the presented research and excellent collaboration and communication of RB. RB and SS acknowledge the infrastructure and stay support provided by DBT-TDNBC-DEAKIN-Research Network Across continents for learning and innovation (DTD-RNA) for AMF-related work at The Energy and Resources Institute, TERI, India. JHC was grateful to CNPq for the researcher fellowship (CNPq grant 309795/2017-6). KT was grateful to CNPq for the doctoral fellowship. BA-S was grateful to SK for his support in facilitating the coordination of the Indian FunCROP team. CN acknowledges the international scientific network BIOALI-CYTED, which contributed to establish FunCROP contacts. BA-S wants to acknowledge especially the extraordinary engagement of CN for online collaboration with RB on data evaluation and presentation and overall manuscript discussion. BA-S appreciates the collaboration of LIVESEED partners with seed material and information on this material and thanks for supporting EM (European Horizon 2020 project LIVESEED Grant No. 727230).Frontiers Media2022-12-27T16:50:53Z2022-12-272021-10-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://hdl.handle.net/10174/32899http://hdl.handle.net/10174/32899https://doi.org/10.3389/fpls.2021.686274engBharadwaj R, Noceda C, Mohanapriya G, Kumar SR, Thiers KLL, Costa JH, Macedo ES, Kumari A, Gupta KJ, Srivastava S, Adholeya A, Oliveira M, Velada I, Sircar D, Sathishkumar R and Arnholdt-Schmitt B (2021) Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness. Front. Plant Sci. 12:686274. doi: 10.3389/fpls.2021.686274https://www.frontiersin.org/articles/10.3389/fpls.2021.686274/fullndndndndndndndndndndndmmo@uevora.ptndndrsathish@buc.edu.inbiarnaflora@gmail.com584Bharadwaj, RevuruNoceda, CarlosMohanapriya, GunasekharanKumar, Sarma RajeevThiers, Karine Leitão LimaCosta, José HélioMacedo, Elisete SantosKumari, AprajitaGupta, Kapuganti JagadisSrivastava, ShivaniAdholeya, AlokOliveira, ManuelaVelada, IsabelSircar, DebabrataSathishkumar, RamalingamArnholdt-Schmitt, Birgitinfo:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2024-01-03T19:33:35Zoai:dspace.uevora.pt:10174/32899Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-20T01:21:38.647324Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
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 |
spellingShingle |
Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness Bharadwaj, Revuru seed quality ROS Warburg effect bacterial endophytes and mycorrhizal fungi organic seeds biotic stress on-farm seed selection |
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_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_sort |
Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness |
author |
Bharadwaj, Revuru |
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_role |
author |
author2 |
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 |
author2_role |
author author author author author author author author author author author author author author author |
dc.contributor.author.fl_str_mv |
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 |
dc.subject.por.fl_str_mv |
seed quality ROS Warburg effect bacterial endophytes and mycorrhizal fungi organic seeds biotic stress on-farm seed selection |
topic |
seed quality ROS Warburg effect bacterial endophytes and mycorrhizal fungi organic seeds biotic stress on-farm seed selection |
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. |
publishDate |
2021 |
dc.date.none.fl_str_mv |
2021-10-01T00:00:00Z 2022-12-27T16:50:53Z 2022-12-27 |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/10174/32899 http://hdl.handle.net/10174/32899 https://doi.org/10.3389/fpls.2021.686274 |
url |
http://hdl.handle.net/10174/32899 https://doi.org/10.3389/fpls.2021.686274 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Bharadwaj R, Noceda C, Mohanapriya G, Kumar SR, Thiers KLL, Costa JH, Macedo ES, Kumari A, Gupta KJ, Srivastava S, Adholeya A, Oliveira M, Velada I, Sircar D, Sathishkumar R and Arnholdt-Schmitt B (2021) Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness. Front. Plant Sci. 12:686274. doi: 10.3389/fpls.2021.686274 https://www.frontiersin.org/articles/10.3389/fpls.2021.686274/full nd nd nd nd nd nd nd nd nd nd nd mmo@uevora.pt nd nd rsathish@buc.edu.in biarnaflora@gmail.com 584 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.publisher.none.fl_str_mv |
Frontiers Media |
publisher.none.fl_str_mv |
Frontiers Media |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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