Cargando…

Isoprene enhances leaf cytokinin metabolism and induces early senescence

Isoprene, a major biogenic volatile hydrocarbon of climate‐relevance, indisputably mitigates abiotic stresses in emitting plants. However functional relevance of constitutive isoprene emission in unstressed plants remains contested. Isoprene and cytokinins (CKs) are synthesized from a common substra...

Descripción completa

Detalles Bibliográficos
Autores principales: Dani, Kaidala Ganesha Srikanta, Pollastri, Susanna, Pinosio, Sara, Reichelt, Michael, Sharkey, Thomas D., Schnitzler, Jörg‐Peter, Loreto, Francesco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9300082/
https://www.ncbi.nlm.nih.gov/pubmed/34716577
http://dx.doi.org/10.1111/nph.17833
_version_ 1784751127988797440
author Dani, Kaidala Ganesha Srikanta
Pollastri, Susanna
Pinosio, Sara
Reichelt, Michael
Sharkey, Thomas D.
Schnitzler, Jörg‐Peter
Loreto, Francesco
author_facet Dani, Kaidala Ganesha Srikanta
Pollastri, Susanna
Pinosio, Sara
Reichelt, Michael
Sharkey, Thomas D.
Schnitzler, Jörg‐Peter
Loreto, Francesco
author_sort Dani, Kaidala Ganesha Srikanta
collection PubMed
description Isoprene, a major biogenic volatile hydrocarbon of climate‐relevance, indisputably mitigates abiotic stresses in emitting plants. However functional relevance of constitutive isoprene emission in unstressed plants remains contested. Isoprene and cytokinins (CKs) are synthesized from a common substrate and pathway in chloroplasts. It was postulated that isoprene emission may affect CK‐metabolism. Using transgenic isoprene‐emitting (IE) Arabidopsis and isoprene nonemitting (NE) RNA‐interference grey poplars (paired with respective NE and IE genotypes), the life of individual IE and NE leaves from emergence to abscission was followed under stress‐free conditions. We monitored plant growth rate, aboveground developmental phenotype, modelled leaf photosynthetic energy status, quantified the abundance of leaf CKs, analysed Arabidopsis and poplar leaf transcriptomes by RNA‐sequencing in presence and absence of isoprene during leaf senescence. Isoprene emission by unstressed leaves enhanced the abundance of CKs (isopentenyl adenine and its precursor) by > 200%, significantly upregulated genes coding for CK‐synthesis, CK‐signalling and CK‐degradation, hastened plant development, increased chloroplast metabolic rate, altered photosynthetic energy status, induced early leaf senescence in both Arabidopsis and poplar. IE leaves senesced sooner even in decapitated poplars where source–sink relationships and hormone homeostasis were perturbed. Constitutive isoprene emission significantly accelerates CK‐led leaf and organismal development and induces early senescence independent of growth constraints. Isoprene emission provides an early‐riser evolutionary advantage and shortens lifecycle duration to assist rapid diversification in unstressed emitters.
format Online
Article
Text
id pubmed-9300082
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-93000822022-07-21 Isoprene enhances leaf cytokinin metabolism and induces early senescence Dani, Kaidala Ganesha Srikanta Pollastri, Susanna Pinosio, Sara Reichelt, Michael Sharkey, Thomas D. Schnitzler, Jörg‐Peter Loreto, Francesco New Phytol Research Isoprene, a major biogenic volatile hydrocarbon of climate‐relevance, indisputably mitigates abiotic stresses in emitting plants. However functional relevance of constitutive isoprene emission in unstressed plants remains contested. Isoprene and cytokinins (CKs) are synthesized from a common substrate and pathway in chloroplasts. It was postulated that isoprene emission may affect CK‐metabolism. Using transgenic isoprene‐emitting (IE) Arabidopsis and isoprene nonemitting (NE) RNA‐interference grey poplars (paired with respective NE and IE genotypes), the life of individual IE and NE leaves from emergence to abscission was followed under stress‐free conditions. We monitored plant growth rate, aboveground developmental phenotype, modelled leaf photosynthetic energy status, quantified the abundance of leaf CKs, analysed Arabidopsis and poplar leaf transcriptomes by RNA‐sequencing in presence and absence of isoprene during leaf senescence. Isoprene emission by unstressed leaves enhanced the abundance of CKs (isopentenyl adenine and its precursor) by > 200%, significantly upregulated genes coding for CK‐synthesis, CK‐signalling and CK‐degradation, hastened plant development, increased chloroplast metabolic rate, altered photosynthetic energy status, induced early leaf senescence in both Arabidopsis and poplar. IE leaves senesced sooner even in decapitated poplars where source–sink relationships and hormone homeostasis were perturbed. Constitutive isoprene emission significantly accelerates CK‐led leaf and organismal development and induces early senescence independent of growth constraints. Isoprene emission provides an early‐riser evolutionary advantage and shortens lifecycle duration to assist rapid diversification in unstressed emitters. John Wiley and Sons Inc. 2021-12-20 2022-05 /pmc/articles/PMC9300082/ /pubmed/34716577 http://dx.doi.org/10.1111/nph.17833 Text en © 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Dani, Kaidala Ganesha Srikanta
Pollastri, Susanna
Pinosio, Sara
Reichelt, Michael
Sharkey, Thomas D.
Schnitzler, Jörg‐Peter
Loreto, Francesco
Isoprene enhances leaf cytokinin metabolism and induces early senescence
title Isoprene enhances leaf cytokinin metabolism and induces early senescence
title_full Isoprene enhances leaf cytokinin metabolism and induces early senescence
title_fullStr Isoprene enhances leaf cytokinin metabolism and induces early senescence
title_full_unstemmed Isoprene enhances leaf cytokinin metabolism and induces early senescence
title_short Isoprene enhances leaf cytokinin metabolism and induces early senescence
title_sort isoprene enhances leaf cytokinin metabolism and induces early senescence
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9300082/
https://www.ncbi.nlm.nih.gov/pubmed/34716577
http://dx.doi.org/10.1111/nph.17833
work_keys_str_mv AT danikaidalaganeshasrikanta isopreneenhancesleafcytokininmetabolismandinducesearlysenescence
AT pollastrisusanna isopreneenhancesleafcytokininmetabolismandinducesearlysenescence
AT pinosiosara isopreneenhancesleafcytokininmetabolismandinducesearlysenescence
AT reicheltmichael isopreneenhancesleafcytokininmetabolismandinducesearlysenescence
AT sharkeythomasd isopreneenhancesleafcytokininmetabolismandinducesearlysenescence
AT schnitzlerjorgpeter isopreneenhancesleafcytokininmetabolismandinducesearlysenescence
AT loretofrancesco isopreneenhancesleafcytokininmetabolismandinducesearlysenescence