Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases

Mor Tsamir-Rimon; Shifra Ben-Dor; Ester Feldmesser; Yaara Oppenhimer-Shaanan; Rakefet David-Schwartz; Alon Samach; Tamir Klein

doi:10.1111/nph.16907

Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases

Mor Tsamir-Rimon, Shifra Ben-Dor, Ester Feldmesser, Yaara Oppenhimer-Shaanan, Rakefet David-Schwartz, Alon Samach, Tamir Klein^*

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

Research output: Contribution to journal › Article › peer-review

19 Scopus citations

Abstract

Carbon reserve use is a major drought response in trees, enabling tree survival in conditions prohibiting photosynthesis. However, regulation of starch metabolism under drought at the whole-tree scale is still poorly understood. To this end, we combined measurements of nonstructural carbohydrates (NSCs), tree physiology and gene expression. The experiment was conducted outside on olive trees in pots under 90 d of seasonal spring to summer warming. Half of the trees were also subjected to limited water conditions for 28 d. Photosynthesis decreased in dehydrating trees from 19 to 0.5 µmol m⁻² s⁻¹ during the drought period. Starch degradation and mannitol production were a major drought response, with mannitol increasing to 71% and 41% out of total NSCs in shoots and roots, respectively. We identified the gene family members potentially relevant either to long-term or stress-induced carbon storage. Partitioning of expression patterns among β amylase and starch synthase family members was observed, with three β amylases possibly facilitating the rapid starch degradation under heat and drought. Our results suggest a group of stress-related, starch metabolism genes, correlated with NSC fluctuations during drought and recovery. The daily starch metabolism gene expression was different from the stress-mode starch metabolism pattern, where some genes are uniquely expressed during the stress-mode response.

Original language	American English
Pages (from-to)	1398-1414
Number of pages	17
Journal	New Phytologist
Volume	229
Issue number	3
DOIs	https://doi.org/10.1111/nph.16907
State	Published - Feb 2021

Bibliographical note

Funding Information:
The authors thank the Merle S. Cahn Foundation; the Monroe and Marjorie Burk Fund for Alternative Energy Studies; Mr and Mrs Norman Reiser; the Weizmann Center for New Scientists; the estate of Helen Nichunsky; the Benoziyo Endowment Fund for the Advancement of Science; and the Edith & Nathan Goldberg Career Development Chair. MT is grateful for the support of the Women’s League of Israel, with scholarships provided during her MSc research. The authors declare no competing interest in the preparation of this manuscript.

Funding Information:
The authors are grateful to S. Wolf and N. Glanz (Hebrew University), for the HPLC analysis; to G. Ben-Ari (ARO Volcani Center) for sharing the database of the olive genome and for commenting on an earlier version of the manuscript, together with J. Gruenzweig (Hebrew University); and to the members of the Klein laboratory (Weizmann TreeLab) for helpful discussions and comments. Five anonymous referees are acknowledged for providing useful comments, which improved the article. The authors thank the Merle S. Cahn Foundation; the Monroe and Marjorie Burk Fund for Alternative Energy Studies; Mr and Mrs Norman Reiser; the Weizmann Center for New Scientists; the estate of Helen Nichunsky; the Benoziyo Endowment Fund for the Advancement of Science; and the Edith & Nathan Goldberg Career Development Chair. MT is grateful for the support of the Women?s League of Israel, with scholarships provided during her MSc research. The authors declare no competing interest in the preparation of this manuscript.

Publisher Copyright:
© 2020 The Authors New Phytologist © 2020 New Phytologist Trust

Keywords

carbon source
drought response
drought tolerance
mannitol
starch degradation
starch synthesis

Access to Document

10.1111/nph.16907

Cite this

@article{732028e84c984886bb8f1d2584b2e0c8,

title = "Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases",

abstract = "Carbon reserve use is a major drought response in trees, enabling tree survival in conditions prohibiting photosynthesis. However, regulation of starch metabolism under drought at the whole-tree scale is still poorly understood. To this end, we combined measurements of nonstructural carbohydrates (NSCs), tree physiology and gene expression. The experiment was conducted outside on olive trees in pots under 90 d of seasonal spring to summer warming. Half of the trees were also subjected to limited water conditions for 28 d. Photosynthesis decreased in dehydrating trees from 19 to 0.5 µmol m−2 s−1 during the drought period. Starch degradation and mannitol production were a major drought response, with mannitol increasing to 71% and 41% out of total NSCs in shoots and roots, respectively. We identified the gene family members potentially relevant either to long-term or stress-induced carbon storage. Partitioning of expression patterns among β amylase and starch synthase family members was observed, with three β amylases possibly facilitating the rapid starch degradation under heat and drought. Our results suggest a group of stress-related, starch metabolism genes, correlated with NSC fluctuations during drought and recovery. The daily starch metabolism gene expression was different from the stress-mode starch metabolism pattern, where some genes are uniquely expressed during the stress-mode response.",

keywords = "carbon source, drought response, drought tolerance, mannitol, starch degradation, starch synthesis",

author = "Mor Tsamir-Rimon and Shifra Ben-Dor and Ester Feldmesser and Yaara Oppenhimer-Shaanan and Rakefet David-Schwartz and Alon Samach and Tamir Klein",

note = "Funding Information: The authors thank the Merle S. Cahn Foundation; the Monroe and Marjorie Burk Fund for Alternative Energy Studies; Mr and Mrs Norman Reiser; the Weizmann Center for New Scientists; the estate of Helen Nichunsky; the Benoziyo Endowment Fund for the Advancement of Science; and the Edith & Nathan Goldberg Career Development Chair. MT is grateful for the support of the Women{\textquoteright}s League of Israel, with scholarships provided during her MSc research. The authors declare no competing interest in the preparation of this manuscript. Funding Information: The authors are grateful to S. Wolf and N. Glanz (Hebrew University), for the HPLC analysis; to G. Ben-Ari (ARO Volcani Center) for sharing the database of the olive genome and for commenting on an earlier version of the manuscript, together with J. Gruenzweig (Hebrew University); and to the members of the Klein laboratory (Weizmann TreeLab) for helpful discussions and comments. Five anonymous referees are acknowledged for providing useful comments, which improved the article. The authors thank the Merle S. Cahn Foundation; the Monroe and Marjorie Burk Fund for Alternative Energy Studies; Mr and Mrs Norman Reiser; the Weizmann Center for New Scientists; the estate of Helen Nichunsky; the Benoziyo Endowment Fund for the Advancement of Science; and the Edith & Nathan Goldberg Career Development Chair. MT is grateful for the support of the Women?s League of Israel, with scholarships provided during her MSc research. The authors declare no competing interest in the preparation of this manuscript. Publisher Copyright: {\textcopyright} 2020 The Authors New Phytologist {\textcopyright} 2020 New Phytologist Trust",

year = "2021",

month = feb,

doi = "10.1111/nph.16907",

language = "American English",

volume = "229",

pages = "1398--1414",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "3",

}

TY - JOUR

T1 - Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases

AU - Tsamir-Rimon, Mor

AU - Ben-Dor, Shifra

AU - Feldmesser, Ester

AU - Oppenhimer-Shaanan, Yaara

AU - David-Schwartz, Rakefet

AU - Samach, Alon

AU - Klein, Tamir

N1 - Funding Information: The authors thank the Merle S. Cahn Foundation; the Monroe and Marjorie Burk Fund for Alternative Energy Studies; Mr and Mrs Norman Reiser; the Weizmann Center for New Scientists; the estate of Helen Nichunsky; the Benoziyo Endowment Fund for the Advancement of Science; and the Edith & Nathan Goldberg Career Development Chair. MT is grateful for the support of the Women’s League of Israel, with scholarships provided during her MSc research. The authors declare no competing interest in the preparation of this manuscript. Funding Information: The authors are grateful to S. Wolf and N. Glanz (Hebrew University), for the HPLC analysis; to G. Ben-Ari (ARO Volcani Center) for sharing the database of the olive genome and for commenting on an earlier version of the manuscript, together with J. Gruenzweig (Hebrew University); and to the members of the Klein laboratory (Weizmann TreeLab) for helpful discussions and comments. Five anonymous referees are acknowledged for providing useful comments, which improved the article. The authors thank the Merle S. Cahn Foundation; the Monroe and Marjorie Burk Fund for Alternative Energy Studies; Mr and Mrs Norman Reiser; the Weizmann Center for New Scientists; the estate of Helen Nichunsky; the Benoziyo Endowment Fund for the Advancement of Science; and the Edith & Nathan Goldberg Career Development Chair. MT is grateful for the support of the Women?s League of Israel, with scholarships provided during her MSc research. The authors declare no competing interest in the preparation of this manuscript. Publisher Copyright: © 2020 The Authors New Phytologist © 2020 New Phytologist Trust

PY - 2021/2

Y1 - 2021/2

N2 - Carbon reserve use is a major drought response in trees, enabling tree survival in conditions prohibiting photosynthesis. However, regulation of starch metabolism under drought at the whole-tree scale is still poorly understood. To this end, we combined measurements of nonstructural carbohydrates (NSCs), tree physiology and gene expression. The experiment was conducted outside on olive trees in pots under 90 d of seasonal spring to summer warming. Half of the trees were also subjected to limited water conditions for 28 d. Photosynthesis decreased in dehydrating trees from 19 to 0.5 µmol m−2 s−1 during the drought period. Starch degradation and mannitol production were a major drought response, with mannitol increasing to 71% and 41% out of total NSCs in shoots and roots, respectively. We identified the gene family members potentially relevant either to long-term or stress-induced carbon storage. Partitioning of expression patterns among β amylase and starch synthase family members was observed, with three β amylases possibly facilitating the rapid starch degradation under heat and drought. Our results suggest a group of stress-related, starch metabolism genes, correlated with NSC fluctuations during drought and recovery. The daily starch metabolism gene expression was different from the stress-mode starch metabolism pattern, where some genes are uniquely expressed during the stress-mode response.

AB - Carbon reserve use is a major drought response in trees, enabling tree survival in conditions prohibiting photosynthesis. However, regulation of starch metabolism under drought at the whole-tree scale is still poorly understood. To this end, we combined measurements of nonstructural carbohydrates (NSCs), tree physiology and gene expression. The experiment was conducted outside on olive trees in pots under 90 d of seasonal spring to summer warming. Half of the trees were also subjected to limited water conditions for 28 d. Photosynthesis decreased in dehydrating trees from 19 to 0.5 µmol m−2 s−1 during the drought period. Starch degradation and mannitol production were a major drought response, with mannitol increasing to 71% and 41% out of total NSCs in shoots and roots, respectively. We identified the gene family members potentially relevant either to long-term or stress-induced carbon storage. Partitioning of expression patterns among β amylase and starch synthase family members was observed, with three β amylases possibly facilitating the rapid starch degradation under heat and drought. Our results suggest a group of stress-related, starch metabolism genes, correlated with NSC fluctuations during drought and recovery. The daily starch metabolism gene expression was different from the stress-mode starch metabolism pattern, where some genes are uniquely expressed during the stress-mode response.

KW - carbon source

KW - drought response

KW - drought tolerance

KW - mannitol

KW - starch degradation

KW - starch synthesis

UR - http://www.scopus.com/inward/record.url?scp=85091768482&partnerID=8YFLogxK

U2 - 10.1111/nph.16907

DO - 10.1111/nph.16907

M3 - Article

C2 - 32880972

AN - SCOPUS:85091768482

SN - 0028-646X

VL - 229

SP - 1398

EP - 1414

JO - New Phytologist

JF - New Phytologist

IS - 3

ER -

Rapid starch degradation in the wood of olive trees under heat and drought is permitted by three stress-specific beta amylases

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Cite this