Abstract
Physical damage can strongly affect plant growth, reducing the biomass of developing organs situated at a distance from wounds. These effects, previously studied in leaves, require the activation of jasmonate (JA) signalling. Using a novel assay involving repetitive cotyledon wounding in Arabidopsis seedlings, we uncovered a function of JA in suppressing cell division and elongation in roots. Regulatory JA signalling components were then manipulated to delineate their relative impacts on root growth. The new transcription factor mutant myc2-322B was isolated. In vitro transcription assays and whole-plant approaches revealed that myc2-322B is a dosage-dependent gain-of-function mutant that can amplify JA growth responses. Moreover, myc2-322B displayed extreme hypersensitivity to JA that totally suppressed root elongation. The mutation weakly reduced root growth in undamaged plants but, when the upstream negative regulator NINJA was genetically removed, myc2-322B powerfully repressed root growth through its effects on cell division and cell elongation. Furthermore, in a JA-deficient mutant background, ninja1 myc2-322B still repressed root elongation, indicating that it is possible to generate JA-responses in the absence of JA. We show that NINJA forms a broadly expressed regulatory layer that is required to inhibit JA signalling in the apex of roots grown under basal conditions. By contrast, MYC2, MYC3 and MYC4 displayed cell layer-specific localisations and MYC3 and MYC4 were expressed in mutually exclusive regions. In nature, growing roots are likely subjected to constant mechanical stress during soil penetration that could lead to JA production and subsequent detrimental effects on growth. Our data reveal how distinct negative regulatory layers, including both NINJA-dependent and -independent mechanisms, restrain JA responses to allow normal root growth. Mechanistic insights from this work underline the importance of mapping JA signalling components to specific cell types in order to understand and potentially engineer the growth reduction that follows physical damage.
Highlights
The development, architecture and mass of nascent plant organs are plastic and can be strongly influenced by injury to pre-existing tissues
We investigated root growth responses at the seedling stage where mechanical wounding of shoots is known to trigger JA signalling in belowground tissues [7, 26]
As there was no information on the spatial organization of JA signalling in the root meristem, which could potentially mediate root growth responses after cotyledon wounding, we investigated the expression domain of NINJA, the only JA-signalling component affecting root growth in undamaged plants [7], and MYC transcription factors (TFs) (MYC2, MYC3 and MYC4) known to have a role in the inhibition of root elongation when seedlings are grown in the presence of exogenous JA [19]
Summary
The development, architecture and mass of nascent plant organs are plastic and can be strongly influenced by injury to pre-existing tissues. In the case of above ground tissues, most of the growth restriction that occurs subsequently to physical damage depends on the activation of the jasmonate (JA) pathway [2,3,4], which has a pivotal role in controlling herbivoreinducible gene expression and coordinating resource allocation between defence and growth [5, 6]. In contrast to the observation of JA-mediated growth restriction in leaves, root growth responses following damage to aerial organs are so far, not clearly understood. There is relatively little knowledge of the cellular organization of JA signalling components in roots. What has emerged to date, is that the same basic JA signalling components operate in shoots and roots, the genetic architecture of the JA pathway appears to be simpler in roots [7]
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