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Cited by 330Insect-Plant Interactions and ControlPlant Molecular Biology ResearchPlant Stress Responses and Tolerance

The DOI matches its Crossref record; 51 of the 53 references it cites were found in a registry or an index, and 2 are not checked yet.

Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis

Open access
Zhang, Yi, Turner, John G.·2008·PLoS ONE
DOI 10.1371/journal.pone.0003699PMC PMC2577035
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Abstract

When plants are repeatedly injured their growth is stunted and the size of organs such as leaves is greatly reduced. The basis of this effect is not well-understood however, even though it reduces yield of crops injured by herbivory, and produces dramatic effects exemplified in ornamental bonsai plants. We have investigated the genetic and physiological basis of this "bonsai effect" by repeatedly wounding leaves of the model plant Arabidopsis. This treatment stunted growth by 50% and increased the endogenous content of jasmonate (JA), a growth inhibitor, by seven-fold. Significantly, repeated wounding did not stunt the growth of the leaves of mutants unable to synthesise JA, or unable to respond to JA including coi1, jai3, myc2, but not jar1. The stunted growth did not result from reduced cell size, but resulted instead from reduced cell number, and was associated with reduced expression of CycB1;2. Wounding caused systemic disappearance of constitutively expressed JAZ1::GUS. Wounding also activates plant immunity. We show that a gene, 12-oxo-phytodienoate reductase, which catalyses a step in JA biosynthesis, and which we confirm is not required for defence, is however required for wound-induced stunting. Our data suggest that intermediates in the JA biosynthetic pathway activate defence, but a primary function of wound-induced JA is to stunt growth through the suppression of mitosis.

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Figures

Figure 1 JA and the wound signal pathway. Linolenic acid synthesised by fatty acid desaturases (FAD) is released from chloroplast lipid in response to a stress such as wounding or attack by pests and pathogens, and it serves as substrate for jasmonate (JA) biosynthesis. 12-oxophytodienoic acid (OPDA) is sufficient for defence against pests and pathogens. Key enzymes in JA synthesis are allene oxide synthase (AOS) and 12-oxophytodienoate reductase 3 (OPR3). Lower case gene symbols indicate mutants used in this study. JAR1 couples JA to an amino acid which activates a signal pathway, involving COI1, which also contributes to defence. Specific wound responses are activated by a COI1-dependent signal that removes JAZ proteins that suppress the transcription factor MYC2/JIN1, leading to its activation.
Figure 1 JA and the wound signal pathway. Linolenic acid synthesised by fatty acid desaturases (FAD) is released from chloroplast lipid in response to a stress such as wounding or attack by pests and pathogens, and it serves as substrate for jasmonate (JA) biosynthesis. 12-oxophytodienoic acid (OPDA) is sufficient for defence against pests and pathogens. Key enzymes in JA synthesis are allene oxide synthase (AOS) and 12-oxophytodienoate reductase 3 (OPR3). Lower case gene symbols indicate mutants used in this study. JAR1 couples JA to an amino acid which activates a signal pathway, involving COI1, which also contributes to defence. Specific wound responses are activated by a COI1-dependent signal that removes JAZ proteins that suppress the transcription factor MYC2/JIN1, leading to its activation.CC BY · PubMed Central
Figure 2 Effect of wounding on Arabidopsis plants. (A) Leaves were wounded by applying pressure with forceps having serrated teeth, bruising the tissue. For JA determination (Figure 2B) and the wound-induced growth inhibition experiments (Figure and Figure 4), the largest leaf was wounded on each occasion. No leaf was wounded more than once. At the end of the experiment, plant usually had 14–16 leaves, of which 10 were wounded (the size of the wounded leaves varied). (B) JA content in control and wounded Col-gl and aos plants. (C) Quantitative RT-PCR was used to measure expression of VSP1 in untreated controls and wounded Col-gl and aos plants. The VSP1 level was relative to ACTIN2. (D) Eighteen-day-old wild type Col-gl and coi1-1 seedlings containing the 35S::JAZ1::GUS transgene were untreated as control or wounded on a single leaf. GUS activity was detected histochemically one hour afterwards. The wounded leaf is not shown in the images.
Figure 2 Effect of wounding on Arabidopsis plants. (A) Leaves were wounded by applying pressure with forceps having serrated teeth, bruising the tissue. For JA determination (Figure 2B) and the wound-induced growth inhibition experiments (Figure and Figure 4), the largest leaf was wounded on each occasion. No leaf was wounded more than once. At the end of the experiment, plant usually had 14–16 leaves, of which 10 were wounded (the size of the wounded leaves varied). (B) JA content in control and wounded Col-gl and aos plants. (C) Quantitative RT-PCR was used to measure expression of VSP1 in untreated controls and wounded Col-gl and aos plants. The VSP1 level was relative to ACTIN2. (D) Eighteen-day-old wild type Col-gl and coi1-1 seedlings containing the 35S::JAZ1::GUS transgene were untreated as control or wounded on a single leaf. GUS activity was detected histochemically one hour afterwards. The wounded leaf is not shown in the images.CC BY · PubMed Central
Figure 3 Effect of wounding on growth of wild type plants and JA mutants. (A) Thirty-one-day old wild type, aos (in Col-gl background), and opr3 (in Ws background) plants after wounding. Controls are unwounded. (B) Leaf area of unwounded and wounded 31-day-old wild type plants and JA mutants (n≥10). Lines underneath the histogram indicate the same genetic background, Col-0, Col-gl, or Ws. (C) Effect of MeJA on root length and fresh weight of wild type Col-0 and jar1 plants (n≥25). (D) Leaf area of unwounded and wounded 31-day-old wild type Ler and quadruple-DELLA mutant plants (n≥10). (E) Growth rates of control and wounded Col-gl and aos plants. Wounding of plants started on day 21, indicated by the dotted line (n = 12).
Figure 3 Effect of wounding on growth of wild type plants and JA mutants. (A) Thirty-one-day old wild type, aos (in Col-gl background), and opr3 (in Ws background) plants after wounding. Controls are unwounded. (B) Leaf area of unwounded and wounded 31-day-old wild type plants and JA mutants (n≥10). Lines underneath the histogram indicate the same genetic background, Col-0, Col-gl, or Ws. (C) Effect of MeJA on root length and fresh weight of wild type Col-0 and jar1 plants (n≥25). (D) Leaf area of unwounded and wounded 31-day-old wild type Ler and quadruple-DELLA mutant plants (n≥10). (E) Growth rates of control and wounded Col-gl and aos plants. Wounding of plants started on day 21, indicated by the dotted line (n = 12).CC BY · PubMed Central
Figure 4 Histochemical detection of GUS in 31-day-old wild type Col-0 plants containing the CycB1;2::GUS reporter. (A) Untreated plants as control. Inset is an enlarged part of the petiole to indicate the individually stained cells (arrow). (B) Plants wounded on ten successive days. (C) Plants sprayed three times over 10 days with MeJA (100 µM) Numbers indicate leaf number. Scale bar, 1 mm.
Figure 4 Histochemical detection of GUS in 31-day-old wild type Col-0 plants containing the CycB1;2::GUS reporter. (A) Untreated plants as control. Inset is an enlarged part of the petiole to indicate the individually stained cells (arrow). (B) Plants wounded on ten successive days. (C) Plants sprayed three times over 10 days with MeJA (100 µM) Numbers indicate leaf number. Scale bar, 1 mm.CC BY · PubMed Central
Figure 5 Effect of MeJA, IAA, ACC, and SA on growth and GUS expression in wild type Col-0 plants containing CycB1;2::GUS transgene. (A) Four-day-old seedlings were transferred to MS as control or to MS containing MeJA (50 µM), IAA (2 µM), ACC (10 µM) or SA (50 µM) for 10 days. (B) Root length of 14 days old seedlings growing on media containing MeJA, IAA, ACC, and SA. (C) Cyclin index of control and MeJA treated plants from (A). (D) Histochemical detection of GUS in seedlings from (A). Scale bar, 0.5 mm. (E) Twelve-day-old seedlings grown on MS media were transferred to MS as control or to MS containing 50 µM MeJA. GUS was detected histochemically at the indicated intervals after transfer. (F) Twelve-day-old seedlings grown on soil were sprayed with water as control or 500 µM MeJA, and again at the intervals at which samples were taken. GUS activity in the samples was measured by the MUG assay. Data points are means of three samples of 60 seedlings each.
Figure 5 Effect of MeJA, IAA, ACC, and SA on growth and GUS expression in wild type Col-0 plants containing CycB1;2::GUS transgene. (A) Four-day-old seedlings were transferred to MS as control or to MS containing MeJA (50 µM), IAA (2 µM), ACC (10 µM) or SA (50 µM) for 10 days. (B) Root length of 14 days old seedlings growing on media containing MeJA, IAA, ACC, and SA. (C) Cyclin index of control and MeJA treated plants from (A). (D) Histochemical detection of GUS in seedlings from (A). Scale bar, 0.5 mm. (E) Twelve-day-old seedlings grown on MS media were transferred to MS as control or to MS containing 50 µM MeJA. GUS was detected histochemically at the indicated intervals after transfer. (F) Twelve-day-old seedlings grown on soil were sprayed with water as control or 500 µM MeJA, and again at the intervals at which samples were taken. GUS activity in the samples was measured by the MUG assay. Data points are means of three samples of 60 seedlings each.CC BY · PubMed Central
Figure 6 JA and OPDA in defence against Bradysia impatiens, and growth inhibition. (A) Survival of Col-gl, aos, Ws and opr3 plants grown in soil infested with larvae of Bradysia impatiens. Adult flies were introduced at day 14 and survival was counted on day 46. (B) Survival of aos plants grown in soil infested with larvae of Bradysia impatiens as (A) and sprayed with MeJA (100 µM), or OPDA (100 µM), or water as a control at day 30, 32 and 35. (C) Quantitative RT-PCR was used to measure the expression of AOS in Ws and opr3 plants untreated as control or wounded twice on two leaves. The AOS level was relative to ACTIN2. (D) OPDA (100 µM) or MeJA (100 µM) was applied to leaves of wild type and opr3 plants at days 21, 23 and 25. Images are of plants at 31 days. (E) Leaf area of plants from (D). (F) Five-day-old wild type Ws and opr3 plants were transferred to MS as control and MS containing 10 µM MeJA or 10 µM OPDA. Images were taken 7 days after transfer. (G) Length of roots of seedlings from (F) (n≥21).
Figure 6 JA and OPDA in defence against Bradysia impatiens, and growth inhibition. (A) Survival of Col-gl, aos, Ws and opr3 plants grown in soil infested with larvae of Bradysia impatiens. Adult flies were introduced at day 14 and survival was counted on day 46. (B) Survival of aos plants grown in soil infested with larvae of Bradysia impatiens as (A) and sprayed with MeJA (100 µM), or OPDA (100 µM), or water as a control at day 30, 32 and 35. (C) Quantitative RT-PCR was used to measure the expression of AOS in Ws and opr3 plants untreated as control or wounded twice on two leaves. The AOS level was relative to ACTIN2. (D) OPDA (100 µM) or MeJA (100 µM) was applied to leaves of wild type and opr3 plants at days 21, 23 and 25. Images are of plants at 31 days. (E) Leaf area of plants from (D). (F) Five-day-old wild type Ws and opr3 plants were transferred to MS as control and MS containing 10 µM MeJA or 10 µM OPDA. Images were taken 7 days after transfer. (G) Length of roots of seedlings from (F) (n≥21).CC BY · PubMed Central
Figure 7 JA and the wound-induced growth inhibition pathway. COI1, JAZ proteins and MYC2 -but not JAR1- are required for wound-induced growth inhibition. This model branches the signal pathway at JA.
Figure 7 JA and the wound-induced growth inhibition pathway. COI1, JAZ proteins and MYC2 -but not JAR1- are required for wound-induced growth inhibition. This model branches the signal pathway at JA.CC BY · PubMed Central

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Metadata

Authors
Zhang, Y., & Turner, J. G.
Affiliations
University of East Anglia (GB)
Corresponding author
Turner, John G.
ORCID
Zhang, Yi
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2008-11-11
Volume
3
Issue
11
Pages
e3699
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0003699
PMC
PMC2577035
OpenAlex
W2044898641
Semantic Scholar
980f00649db4d7829a199b00da6ed71d0f5ce6d4
Cited by
330
References
52
Citations by year
2026: 17 · 2025: 13 · 2024: 14 · 2023: 12 · 2022: 21 · 2021: 19 · 2020: 20 · 2019: 22 · 2018: 12 · 2017: 26 · 2016: 15 · 2015: 22 · 2014: 24 · 2013: 26 · 2012: 21
FWCI
17.02
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • UEA Digital Repository (University of East Anglia) (submittedVersion)
Funders
  • University of East Anglia
  • University of Leeds
  • China Scholarship Council
  • Biotechnology and Biological Sciences Research Council
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
Keywords
mitosis inhibition, leaf wounding, Arabidopsis thaliana, jasmonate biosynthesis, JAZ1, cyclin B1, plant immunity, herbivory
MeSH terms
Cell Division, Cyclopentanes, Mitosis, Nucleotidyltransferases, Peptide Synthases, Plant Growth Regulators, Signal Transduction, Arabidopsis, Plant Leaves, Arabidopsis Proteins, Basic Helix-Loop-Helix Leucine Zipper Transcription Factors, Oxylipins

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Zhang, Y., & Turner, J. G. (2008). Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis. PLoS ONE. https://doi.org/10.1371/journal.pone.0003699

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