Isoprene enhances leaf cytokinin metabolism and induces early senescence.

biogenic volatiles cytokinins hormones isoprene leaf senescence signalling transcriptomics unstressed plants

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
05 2022
Historique:
received: 14 06 2021
accepted: 22 10 2021
pubmed: 31 10 2021
medline: 2 4 2022
entrez: 30 10 2021
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 34716577
doi: 10.1111/nph.17833
pmc: PMC9300082
doi:

Substances chimiques

Butadienes 0
Cytokinins 0
Hemiterpenes 0
Pentanes 0
isoprene 0A62964IBU

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

961-974

Informations de copyright

© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.

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Auteurs

Kaidala Ganesha Srikanta Dani (KGS)

Institute for Sustainable Plant Protection, National Research Council of Italy, Via Madonna del Piano 10, 50019, Sesto Fiorentino, Florence, Italy.
Department of Biology, Agriculture and Food Sciences, National Research Council of Italy, Piazzale Aldo Moro 7, 00185, Rome, Italy.

Susanna Pollastri (S)

Institute for Sustainable Plant Protection, National Research Council of Italy, Via Madonna del Piano 10, 50019, Sesto Fiorentino, Florence, Italy.

Sara Pinosio (S)

Institute of Biosciences and Bioresources, National Research Council of Italy, Via Madonna del Piano 10, 50019, Sesto Fiorentino, Florence, Italy.
Institute for Applied Genomics, Via Jacopo Linussio 51, 33100, Udine, Italy.

Michael Reichelt (M)

Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Strasse 8, D-07745, Jena, Germany.

Thomas D Sharkey (TD)

MSU-DOE Plant Research Laboratory, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824, USA.

Jörg-Peter Schnitzler (JP)

Research Unit Environmental Simulation, Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764, Neuherberg, Germany.

Francesco Loreto (F)

Department of Biology, Agriculture and Food Sciences, National Research Council of Italy, Piazzale Aldo Moro 7, 00185, Rome, Italy.
Department of Biology, University of Naples Federico II, Via Cinthia, 80126, Naples, Italy.

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