Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effects of polyploidy on photosynthetic properties and anatomy in leaves of Phlox drummondii

Poonam Vyas A B , Madho Singh Bisht C , Shin-Ichi Miyazawa A D , Satoshi Yano A E , Ko Noguchi A F , Ichiro Terashima A F and Sachiko Funayama-Noguchi A F G
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka, Osaka 560-0043, Japan.

B 51-51 (II Floor), Pocket D-1, Sector-XI, Rohini, Delhi 110 085, India.

C Centre for Inter-disciplinary Studies of Mountain and Hill Environment, Academic Research Centre Building, University of Delhi, Patel Marg, Delhi 110 007, India.

D Research Institute of Innovative Technology for the Earth (RITE), 9-2 Kizugawadai, Kizugawa-shi, Kyoto 619-0292, Japan.

E National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki 444-8585, Japan.

F Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.

G Corresponding author. Email: funayama@biol.s.u-tokyo.ac.jp

Functional Plant Biology 34(8) 673-682 https://doi.org/10.1071/FP07020
Submitted: 29 January 2007  Accepted: 15 May 2007   Published: 23 July 2007

Abstract

Polyploidy affects photosynthesis by causing changes in morphology, anatomy and biochemistry. However, in newly developed polyploids, the genome may be unstable. In this study, diploid (2×) and synthetic autotetraploids in initial (4×-C0) and 11th generations (4×-C11) of Phlox drummondii Hook were used to study the effects of chromosome doubling and genome stabilisation on leaf photosynthesis and anatomical properties. The light-saturated photosynthetic rate on a leaf area basis at 360 µmol CO2 mol–1 air (A360) was highest in 4×-C11 leaves, intermediate in 4×-C0 leaves, and lowest in 2× leaves. Rubisco amounts, CO2-saturated photosynthetic rate at 1200 µmol CO2 mol–1 air at PPFD of 1000 µmol m–2 s–1 (A1200, representing the capacity for RuBP regeneration), cumulative surface areas of chloroplasts facing intercellular spaces (Sc), all expressed on a leaf area basis, were all higher in 4× leaves than in 2× leaves, and stomatal conductance (gs) at 360 µmol CO2 mol–1 air was only higher in the 4×-C11 leaves. A360 for the 4×-C11 leaves was greater than that in the 4×-C0 leaves despite having similar amounts of Rubisco. This was presumably associated with a greater RuBP regeneration capacity, as well as an increase in Sc and gs, which would increase the CO2 concentration of Rubisco. These results indicate that the higher rate of photosynthesis in 4×-C11 leaves was not an immediate outcome of chromosome doubling; rather, it was due to adjustment and adaptation during the process of genome stabilisation.

Additional keywords: autopolyploidy, photosynthesis, Rubisco, stomatal conductance.


Acknowledgements

This study was supported by a Fellowship from the Japan Society for the Promotion of Science for foreign researchers to PV. The authors are grateful to the two anonymous reviewers for their constructive comments.


References


Albertin W, Brabant P, Catrice O, Eber F, Jenczewski E, Chevre A-M, Thiellement H (2005) Autopolyploidy in cabbage (Brassica oleraceae L.) does not alter significantly the proteomes of green tissues. Proteomics 5, 2131–2139.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bazzaz FA, Levin DA, Levy M, Schmierbach MR (1982) The effect of chromosome doubling on photosynthetic rates in Phlox. Photosynthetica 17, 89–92. open url image1

Bjurman B (1959) The photosynthesis in diploid and tetraploid Ribes satigrum. Physiologia Plantarum 12, 183–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bretagnolle F, Thompson JD (2001) Phenotypic plasticity in sympatric diploid and autotetraploid Dactylis glomarata. International Journal of Plant Sciences 162, 309–316.
Crossref | GoogleScholarGoogle Scholar | open url image1

Butterfass T (1989) Nuclear control of plastid division. In ‘The division and segregation of organelles’. (Eds SA Boffey, D Lloyd) pp. 21–38. (Cambridge University Press: Cambridge)

Byrne MC, Nelson CJ, Randall DD (1981) Ploidy effects on anatomy and gas exchange of tall fescue leaves. Plant Physiology 68, 891–893.
PubMed |
open url image1

Comai L (2000) Genetic and epigenetic interactions in allopolyploid plants. Plant Molecular Biology 43, 387–399.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dunstone RL, Evans LT (1974) Role of changes in cell size in the evolution of wheat. Australian Journal of Plant Physiology 1, 157–165.
Crossref | GoogleScholarGoogle Scholar | open url image1

Evans JR , Loreto F (2000) Acquisition and diffusion of CO2 in higher plant leaves. In ‘Photosynthesis: physiology and metabolism’. (Eds RC Leegood, TD Sharkey, S von Caemmerer) pp. 321–351. (Kluwer Academic Publishers: Dordrecht)

Frydrych J (1970) Photosynthetic characteristics of diploid and tetraploid forms of Brassica oleracea var. gongylodes grown under different irradiance. Photosynthetica 4, 139–145. open url image1

Funayama S, Terashima I (1997) Photosynthetic properties of leaves of Eupatorium makinoi infected by a geminivirus. Photosynthesis Research 53, 253–261.
Crossref | GoogleScholarGoogle Scholar | open url image1

Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR (1999) Ploidy regulation of gene expression. Science 285, 251–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Givnish TJ (1987) Adaptation to Sun and Shade: A whole-plant perspective. In ‘Ecology of photosynthesis in sun and shade’. (Eds JR Evans, S von Caemmerer, WW Adams III) pp. 63–92. (CSIRO Publishing: Melbourne)

Laemmli UK (1970) Cleavage of structural proteins during the assembly of bacteriophage T4. Nature 227, 680–685.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leech RM, Leese BM, Jellings AJ (1985) Variation in cellular ribulose-1,5-bisphosphate-carboxylase content in leaves of Triticum genotypes at three levels of ploidy. Planta 166, 259–263.
Crossref | GoogleScholarGoogle Scholar | open url image1

Levin DA (1983) Polyploidy and novelty in flowering plants. American Naturalist 122, 1–25.
Crossref | GoogleScholarGoogle Scholar | open url image1

Levin DA, Torres AM, Levy M (1979) Alcohol dehydrogenase activity in diploid and autotetraploid Phlox. Biochemical Genetics 17, 35–42.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Levy M (1976) Altered glycoflavone expression in induced autotetraploids of Phlox drummondii. Biochemical Systematics and Ecology 4, 249–254.
Crossref | GoogleScholarGoogle Scholar | open url image1

Liu B, Wendel JF (2002) Non-Mendelian phenomena in allopolyploid genome evolution. Current Genomics 3, 489–505.
Crossref | GoogleScholarGoogle Scholar | open url image1

Makino A, Mae T, Ohira K (1986) Calorimetric measurement of protein stained with coomassie brilliant blue R on sodium dodecyl sulphate polyacrylamide gel electrophoresis by eluting with formamide. Agricultural and Biological Chemistry 50, 1911–1912. open url image1

Matzke MA, Scheid OM, Matzke AJM (1999) Rapid structural and epigenetic changes in polyploid and aneuploid genomes. BioEssays 21, 761–767.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mauer J, Mayo JM, Denford K (1978) Comparative ecophysiology of the chromosome races in Viola adunca J.E. Smith. Oecologia 35, 91–104.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miyazawa S-I, Terashima I (2001) Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristis and photosynthetic rate. Plant, Cell & Environment 24, 279–291.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mooney HA, Johnson AW (1965) Comparative physiological ecology of an arctic and an alpine population of Thalictrum alpinum L. Ecology 46, 721–727.
Crossref | GoogleScholarGoogle Scholar | open url image1

Naggle GR (1946) The physiology of polyploidy in plants. I. Review of literature. Lloydia 9, 153–173. open url image1

Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant, Cell & Environment 26, 505–512.
Crossref | GoogleScholarGoogle Scholar | open url image1

Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ , et al. (2003) Understanding mechanisms of novel gene expression in polyploids. Trends in Genetics 19, 141–147.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pfeiffer T, Schrader LE, Bingham ET (1980) Physiological comparison of isogenic diploid-tetraploid, tetraploid-octaploid alfalfa populations. Crop Science 20, 299–303. open url image1

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33, 589–639.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reynolds ES (1963) The use of lead citrate at high pH as an electron dense stain for electron microscopy. Journal of Cell Biology 17, 208–212.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Romero-Aranda R, Bondada BR, Syvertsen JP, Grosser JW (1997) Leaf characteristics and net exchange of diploid and autotetraploid Citrus. Annals of Botany 79, 153–160.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schranz ME, Osborn TC (2000) Novel flowering time variation in the resynthesized polyploidy Brassica napus. Journal of Heredity 91, 242–246.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schranz ME, Osborn TC (2004) De novo variation in life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae). American Journal of Botany 91, 174–183. open url image1

Silvertown JW , Lovett Doust J (1993) ‘Introduction to plant population biology.’ (Blackwell Scientific Publications: Oxford)

Sokal RR , Rohlf FJ (1995) ‘Biometry.’ 4th edn. (W.H. Freeman and Company: New York)

Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proceedings of the National Academy of USA 97, 7051–7057.
Crossref | GoogleScholarGoogle Scholar | open url image1

Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 31–43.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stebbins GL (1950) ‘Variation and evolution in plants.’ (Columbia University Press: New York)

Stebbins GL (1971) ‘Chromosomal evolution in higher plants.’ (Addison-Wesley: Reading)

Stempak JC, Ward RT (1964) An improved staining method for electron microscopy. Journal of Cell Biology 22, 697–701.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Syvertsen JP, Lloyd J, McConchi C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant, Cell & Environment 18, 149–157.
Crossref |
open url image1

Terashima I, Miyazawa S-I, Hanba YT (2001) Why are sun leaves thicker than shade leaves? – consideration based on analysis of CO2 diffusion in the leaf. Journal of Plant Research 114, 93–105.
Crossref | GoogleScholarGoogle Scholar | open url image1

Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative ecodevelopment of sun and shade leaves in relation to photosynthetic CO2 diffusion. Journal of Experimental Botany 57, 343–354.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thain JF (1983) Curvature correction factors in the measurement of cell surface areas in plant tissues. Journal of Experimental Botany 34, 87–94.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thompson JD, Lumaret R (1992) The evolutionary dynamics of polyploid plants: origins establishment and persistence. Trends in Ecology & Evolution 7, 302–307.
Crossref | GoogleScholarGoogle Scholar | open url image1

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthsis and the gas exchange of leaves. Planta 153, 376–387.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wang X, Shi X, Hao B, Ge S, Luo J (2005) Duplication and DNA segmental loss in the rice genome implications for diplodization. New Phytologist 165, 937–946.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Warner DA, Edwards GE (1988) C4 photosynthesis and leaf anatomy in diploid and autotetraploid Pennisetum americanum (pearl millet). Plant Science 56, 85–92.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warner DA, Edwards GE (1993) Effects of polyploidy on photosynthesis. Photosynthesis Research 35, 135–147.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warner DA, Ku MSB, Edwards GE (1987) Photosynthesis, leaf anatomy, and cellular constituents in the polyploid C4 grass Panicum virgatum. Plant Physiology 84, 461–466.
PubMed |
open url image1

Watanabe N, Kobayashi S, Furuta Y (1997) Effect of genome and ploidy on photosynthesis. Euphytica 94, 303–309.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wendel JF (2000) Genome evolution in polyploids. Plant Molecular Biology 42, 225–249.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1