Abstract
Phytohormones regulate plant growth from cell division to organ development. Jasmonates (JAs) are signaling molecules that have been implicated in stress-induced responses. However, they have also been shown to inhibit plant growth, but the mechanisms are not well understood. The effects of methyl jasmonate (MeJA) on leaf growth regulation were investigated in Arabidopsis (Arabidopsis thaliana) mutants altered in JA synthesis and perception, allene oxide synthase and coi1-16B (for coronatine insensitive1), respectively. We show that MeJA inhibits leaf growth through the JA receptor COI1 by reducing both cell number and size. Further investigations using flow cytometry analyses allowed us to evaluate ploidy levels and to monitor cell cycle progression in leaves and cotyledons of Arabidopsis and/or Nicotiana benthamiana at different stages of development. Additionally, a novel global transcription profiling analysis involving continuous treatment with MeJA was carried out to identify the molecular players whose expression is regulated during leaf development by this hormone and COI1. The results of these studies revealed that MeJA delays the switch from the mitotic cell cycle to the endoreduplication cycle, which accompanies cell expansion, in a COI1-dependent manner and inhibits the mitotic cycle itself, arresting cells in G1 phase prior to the S-phase transition. Significantly, we show that MeJA activates critical regulators of endoreduplication and affects the expression of key determinants of DNA replication. Our discoveries also suggest that MeJA may contribute to the maintenance of a cellular "stand-by mode" by keeping the expression of ribosomal genes at an elevated level. Finally, we propose a novel model for MeJA-regulated COI1-dependent leaf growth inhibition.
Highlights
Phytohormones regulate plant growth from cell division to organ development
The process of endoreduplication, which is an increase of ploidy levels via rereplication of DNA in the absence of mitosis (M phase), has been associated with cell expansion, where an increased cell volume is driven by internal turgor pressure (SugimotoShirasu and Roberts, 2003)
We measured the leaf area of in vitro-grown Col gl1, coi1-16B, and aos plants, harvesting leaves 1 and 2 at 9, 13, and 19 d after stratification (DAS). This kinematic analysis showed that leaf growth was dramatically inhibited by methyl jasmonate (MeJA) treatment in Col gl1 and aos plants consistently at all stages of development (Fig. 2, A and B; Supplemental Table S1)
Summary
Phytohormones regulate plant growth from cell division to organ development. Jasmonates (JAs) are signaling molecules that have been implicated in stress-induced responses. A novel global transcription profiling analysis involving continuous treatment with MeJA was carried out to identify the molecular players whose expression is regulated during leaf development by this hormone and COI1. The results of these studies revealed that MeJA delays the switch from the mitotic cell cycle to the endoreduplication cycle, which accompanies cell expansion, in a COI1-dependent manner and inhibits the mitotic cycle itself, arresting cells in G1 phase prior to the S-phase transition. Several studies involving plant hormones such as auxin (PerrotRechenmann, 2010), abscisic acid (Swiatek et al, 2002; Skirycz and Inzé, 2010), brassinosteroids (Clouse, 2011), GAs (Achard et al, 2009), or cytokinins (Haberer and Kieber, 2002) show how hormonal signaling networks are able to modulate cell division parameters to impact plant growth and development
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