Exaggerated root respiration accounts for growth retardation in a starchless mutant of Arabidopsis thaliana

Plant J. 2014 Jul;79(1):82-91. doi: 10.1111/tpj.12555. Epub 2014 Jun 20.

Abstract

The knock-out mutation of plastidial phosphoglucomutase (pgm) causes a starchless phenotype in Arabidopsis thaliana, and results in a severe growth reduction of plants cultivated under diurnal conditions. It has been speculated that high soluble sugar levels accumulating during the light phase in leaf mesophyll might cause a reduction of photosynthetic activity or that shortage of reduced carbon during the night is the reason for the slow biomass gain of pgm. Separate simultaneous measurements of leaf net photosynthesis and root respiration demonstrate that photosynthetic activity per unit fresh weight is not reduced in pgm, whereas root respiration is strongly elevated. Comparison with a mutant defective in the dominating vacuolar invertase (AtβFruct4) revealed that high sucrose concentration in the cytosol, but not in the vacuole, of leaf cells is responsible for elevated assimilate transport to the root. Increased sugar supply to the root, as observed in pgm mutants, forces substantial respiratory losses. Because root respiration accounts for 80% of total plant respiration under long-day conditions, this gives rise to retarded biomass formation. In contrast, reduced vacuolar invertase activity leads to reduced net photosynthesis in the shoot and lowered root respiration, and affords an increased root/shoot ratio. The results demonstrate that roots have very limited capacity for carbon storage but exert rigid control of supply for their maintenance metabolism.

Keywords: Arabidopsis thaliana; assimilate transport; carbohydrate compartmentation; phosphoglucomutase mutant; root respiration; root/shoot ratio; sink source relation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / physiology*
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Biological Transport
  • Biomass
  • Carbohydrate Metabolism
  • Carbon Dioxide / metabolism*
  • Cell Respiration / physiology*
  • Circadian Rhythm
  • Gene Knockout Techniques
  • Hydroponics
  • Light
  • Mutation
  • Phosphoglucomutase / genetics
  • Phosphoglucomutase / metabolism
  • Photoperiod
  • Photosynthesis / physiology*
  • Plant Leaves / genetics
  • Plant Leaves / growth & development
  • Plant Leaves / physiology
  • Plant Leaves / radiation effects
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / physiology
  • Plant Roots / radiation effects
  • Plant Shoots / genetics
  • Plant Shoots / growth & development
  • Plant Shoots / physiology
  • Plant Shoots / radiation effects
  • Plastids / metabolism
  • Starch / metabolism*
  • beta-Fructofuranosidase / genetics
  • beta-Fructofuranosidase / metabolism

Substances

  • Arabidopsis Proteins
  • Carbon Dioxide
  • Starch
  • beta-Fructofuranosidase
  • Phosphoglucomutase