Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2013 Oct;25(10):3760-9.
doi: 10.1105/tpc.113.115519. Epub 2013 Oct 4.

Nighttime Sugar Starvation Orchestrates Gibberellin Biosynthesis and Plant Growth in Arabidopsis

Affiliations
Free PMC article

Nighttime Sugar Starvation Orchestrates Gibberellin Biosynthesis and Plant Growth in Arabidopsis

Eleonora Paparelli et al. Plant Cell. .
Free PMC article

Abstract

A plant's eventual size depends on the integration of its genetic program with environmental cues, which vary on a daily basis. Both efficient carbon metabolism and the plant hormone gibberellin are required to guarantee optimal plant growth. Yet, little is known about the interplay between carbon metabolism and gibberellins that modulates plant growth. Here, we show that sugar starvation in Arabidopsis thaliana arising from inefficient starch metabolism at night strongly reduces the expression of ent-kaurene synthase, a key regulatory enzyme for gibberellin synthesis, the following day. Our results demonstrate that plants integrate the efficiency of photosynthesis over a period of days, which is transduced into a daily rate of gibberellin biosynthesis. This enables a plant to grow to a size that is compatible with its environment.

Figures

Figure 1.
Figure 1.
GAs Rescue the Dwarf Phenotype of Starch Mutants to a Large Extent. (A) Representative growth phenotypes of wild-type (Col-0), pgm, and sex1-1 plants from 14 to 35 d after germination. Bar = 1.5 cm. (B) Effect of GA4+7 application on growth of wild-type (Col-0), pgm, adg1-1, sex1-1, sex4-3, and lsf1-1 plants. (C) Rosette size of Col-0 and mutants in absence (−GA4+7) or presence (+GA4+7) of 10 µM GA4+7. Data are mean values of 10 replicates ± sd (two-way analysis of variance; ***P < 0.001).
Figure 2.
Figure 2.
Alterations in Starch Metabolism Affect GA Biosynthesis. (A) Pathways of GA synthesis in Arabidopsis. The enzymes involved are ent-copalyl diphosphate (CPS), ent-kaurene synthase (KS), ent-kaurene oxidase (KO), ent-kaurenoic acid oxidase (KAO), GA20-oxidase (GA20ox), GA3-oxidase (GA3ox), and GA2-oxidase (GA2ox). (B) Diurnal changes in the relative expression levels of genes involved in the GA biosynthetic pathway in Col-0, pgm, and sex1-1 plants grown under a 12-h-light/12-h-dark photoperiod. Expression levels are expressed as relative units assuming as unitary the value of the wild type (Col-0) at the beginning of the day (0 h). Yellow background, day; gray background, night. (C) Endogenous level of ent-kaurene (ng g−1 fresh weight [FW]) in Col-0, pgm, and sex1-1 at the end of night (8 am) and day (8 pm). Asterisks indicate significant differences from the wild type (two-way analysis of variance; **P < 0.01 and ***P < 0.001). (D) Level of GAs (ng g−1 fresh weight) in Col-0, pgm, and sex1-1 at the end of day (8 pm). Values are means (±sd) of three independent replicates.
Figure 3.
Figure 3.
Reduction in KS Expression Level in RNAi Knockdown Lines Results in Decreased Rosette Diameter. (A) Representative growth phenotypes of 4-week-old Col-0 (WT) and selected KSi lines and pgm and sex1-1 plants. Bar = 1.5 cm. (B) Correlation between the rosette diameter (y axis) and KS expression levels (x axis) of wild-type Col-0 (green symbols), KSi knockdown lines (closed symbols), pgm (red symbol), and sex1-1 (blue symbol) mutants. For pictures and transcript levels of the complete set of plants, see Supplemental Figure 7 online.
Figure 4.
Figure 4.
Relationship between Night Starvation and Expression of KS during the Following Light Period. (A) Pathway of starch synthesis and degradation in Arabidopsis leaves. The enzymatic steps affected by each mutation are indicated. (B) and (C) Comparisons of the expression of KS and the starvation reporter gene (DIN6) in Col-0 and starch mutants analyzed in a 12-h-light/12-h-dark photoperiod (gray/yellow background corresponds to night/day). The relative expression level (REL) at the end of night of the wild type (Col-0) was set to 1. (D) and (E) Transcript levels of KS in Col-0, sex1-1 (D), and pgm (E) mutants treated with 1% Suc starting 13 h before dawn (closed symbols). Control plants (open symbols) were sprayed with water. The relative expression level at the end of night of the wild type (Col-0) was set to 1. Values are means (±sd) of three replicates from a single experiment. An independent experiment gave comparable results.
Figure 5.
Figure 5.
Higher Light Intensity Reduces Starvation Symptoms at Night and Restores KS Expression. (A) Phenotype of Col-0, pgm, and sex1-1 plants at 100 or 200 µmol m−2 s−1 light intensity. (B) Transcript levels of KS and DIN6 in Col-0, pgm, and sex1-1 plants at 100 or 200 µmol m−2 s−1 light intensity. The relative expression level (REL) at the end of night (hour 8) of the wild type (Col-0) was set to 1. (C) Level of GAs (ng g−1 fresh weight [FW]) in Col-0, pgm, and sex1-1 grown at 200 µmol m−2 s−1 light intensity at the end of day (8 pm). Values are means (±sd) of three independent replicates.
Figure 6.
Figure 6.
KS Expression Is Adjusted to Unexpected Changes in Light Intensity during the Previous Day. (A) Col-0 plants grown in a 12-h-light/12-h-dark photoperiod at 100 µmol m−2 s−1 light intensity were used as controls. D, day; N, night. (B) Another group of plants was subjected to a 12-h treatment at low-light intensity (10 µmol m−2 s−1; light-gray background) and then transferred to normal light intensity (yellow background). DIN6, KS, GA20ox, EXP10, and EXP1 expression analysis over 3 d was performed. Expression in the control set of plants (A) at time 0 was set to 1. Pictures show Lugol’s staining of a representative plant at the end of the first day. (C) and (D) Leaf elongation under the experimental conditions described in (A) and (B), respectively. Values are means (±sd) of three replicates from two independent experiments.
Figure 7.
Figure 7.
Model Depicting the Regulation of Growth by Sugar Starvation and GAs. Growth at night requires both the presence of transitory starch and the synthesis of GAs. Should photosynthesis be unable to provide enough starch to support growth at night, a starvation signal will be generated that downregulates the synthesis of GAs the next day to balance the hormone-driven growth with the lower carbon availability.

Similar articles

See all similar articles

Cited by 24 articles

See all "Cited by" articles

Publication types

MeSH terms

LinkOut - more resources

Feedback