Elevated CO2 induces age-dependent restoration of growth and metabolism in gibberellin-deficient plants
The effect of elevated [CO2] on the growth of tomato plants with reduced gibberellin content is influenced by developmental stage.
The impact of increased atmospheric carbon dioxide (CO2) on plants has aroused interest in the last decades. Signaling molecules known as plant hormones are fundamental controllers of plant growth and development. Elevated CO2 concentration ([CO2]) increases plant growth; however, whether plant hormones act as mediators of this effect is still an open question. Here, we show the response to elevated [CO2] in tomato does not require a functional gibberellin (GA) biosynthesis pathway. We compared growth and primary metabolism between wild-type (WT) and GA-deficient mutant (gib-1) plants transferred from ambient (400 ppm) to elevated (750 ppm) [CO2] at two different growth stages (either 21 or 35 days after germination, DAG). Growth, photosynthetic parameters and primary metabolism in the stunted gib-1 plants were restored when they were transferred to elevated [CO2] at 21 DAG. Elevated [CO2] also stimulated growth and photosynthetic parameters in WT plants at 21 DAG; however, only minor changes were observed in the level of primary metabolites. At 35 DAG, on the other hand, elevated [CO2] did not stimulate growth in WT plants and gib-1 mutants showed their characteristic stunted growth phenotype. Taken together, our results reveal that elevated [CO2] enhances growth only within a narrow developmental window, in which GA biosynthesis is dispensable. This finding could be relevant for breeding crops in the face of the expected increases in atmospheric CO2 over the next century.
KeywordsCell division Elevated CO2 Phase transition Plant hormone Tomato gibberellin-deficient 1 mutant
Net rate of carbon assimilation
Days after germination
Relative growth ratio
Specific leaf area
This work was funded by a Grant (443064/2014–8) from the National Council for Scientific and Technological Development (CNPq, Brazil). This study was financed in part by the Coordination for the Improvement of Higher-Level Personnel (CAPES-Brazil) (Finance Code 001). We thank Joaquim Gasparini for assistance with photos.
- Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372. https://doi.org/10.1111/j.1469-8137.2004.01224.x CrossRefGoogle Scholar
- Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling heterotrophic cells. Planta 212:250–263. https://doi.org/10.1007/s004250000386 CrossRefGoogle Scholar
- Gibon Y, Blaesing OE, Hannemann J et al (2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16:3304–3325. https://doi.org/10.1105/tpc.104.025973 CrossRefGoogle Scholar
- Hedden P, Thomas SG (eds) (2016) The gibberellins. Annual Plant Reviews, 49, Wiley, ChichesterGoogle Scholar
- Hunt R (1982) Plant growth curves. The functional approach to plant growth analysis. Edward Arnold Ltd., LondonGoogle Scholar
- Johansen DA (1940) Plant microtechnique. McGraw-Hill Publishing Company, Ltd., LondonGoogle Scholar
- Kimura S, Sinha N (2008) Tomato (Solanum lycopersicum): a model fruit-bearing crop. CSH Protoc 2008:pdb.emo105Google Scholar
- Nagel OW, Konings H, Lambers H (2001) The influence of a reduced gibberellin biosynthesis and nitrogen supply on the morphology and anatomy of leaves and roots of tomato (Solanum lycopersicum). Physiol Plant 111:40–45. https://doi.org/10.1034/j.1399-3054.2001.1110106.x CrossRefGoogle Scholar
- Poethig RS (2013) Vegetative phase change and shoot maturation in plants, 1st edn. Elsevier Inc., AmsterdamGoogle Scholar
- Poorter H, van der Werf A (1998) Is inherent variation in RGR determined by LAR at low light and by NAR at high light? A review of herbaceous species. In: Lambers H, Pooter H, Vuuren MMI (eds) Inherent variation in plant growth. Backhuys Publishers, Leiden, Physiological mechanisms and ecological consequences, pp 309–336Google Scholar
- Slafer GA (2003) Genetic basis of yield as viewed from a crop physiologist’s perspective. Ann Appl Biol 142:117–128. https://doi.org/10.1111/j.1744-7348.2003.tb00237.x CrossRefGoogle Scholar
- Vicente MH, Zsögön A, de Sá AFL et al (2015) Semi-determinate growth habit adjusts the vegetative-to-reproductive balance and increases productivity and water-use efficiency in tomato (Solanum lycopersicum). J Plant Physiol 177:11–19. https://doi.org/10.1016/j.jplph.2015.01.003 CrossRefGoogle Scholar
- Watanabe CK, Sato S, Yanagisawa S et al (2014) Effects of elevated CO2 on levels of primary metabolites and transcripts of genes encoding respiratory enzymes and their diurnal patterns in Arabidopsis thaliana: possible relationships with respiratory rates. Plant Cell Physiol 55:341–357. https://doi.org/10.1093/pcp/pct185 CrossRefGoogle Scholar
- Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804 CrossRefGoogle Scholar