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Physiology and Molecular Biology of Plants logoLink to Physiology and Molecular Biology of Plants
. 2008 Sep 27;14(3):253–271. doi: 10.1007/s12298-008-0024-0

Respiration hastens maturation and lowers yield in rice

V Sitaramam 1,, R Bhate 1, P Kamalraj 1, S Pachapurkar 1
PMCID: PMC3550612  PMID: 23572892

Abstract

Role of respiration in plant growth remains an enigma. Growth of meristematic cells, which are not photosynthetic, is entirely driven by endogenous respiration. Does respiration determine growth and size or does it merely burn off the carbon depleting the biomass? We show here that respiration of the germinating rice seed, which is contributed largely by the meristematic cells of the embryo, quantitatively correlates with the dynamics of much of plant growth, starting with the time for germination to the time for flowering and yield. Seed respiration appears to define the quantitative phenotype that contributes to yield via growth dynamics that could be discerned even in commercial varieties, which are biased towards higher yield, despite considerable susceptibility of the dynamics to environmental perturbations. Intrinsic variation, irreducible despite stringent growth conditions, required independent validation of relevant physiological variables both by critical sampling design and by constructing dendrograms for the interrelationships between variables that yield high consensus. More importantly, seed respiration, by mediating the generation clock time via variable time for maturation as seen in rice, directly offers the plausible basis for the phenotypic variation, a major ecological stratagem in a variable environment with uncertain water availability. Faster respiring rice plants appear to complete growth dynamics sooner, mature faster, resulting in a smaller plant with lower yield. Counter to the common allometric views, respiration appears to determine size in the rice plant, and offers a valid physiological means, within the limits of intrinsic variation, to help parental selection in breeding.

Key words: Meristematic cells, allometry, flowering, branching

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Abbreviations

Jo

nmoles of oxygen consumed.min−1.plant−1, specified for individual part of the plant

tg

time taken for 50% germination

tf

time taken for 50% flowering

tlai

time taken for appearance of ith leaf

tlgi

time taken for 50% growth of the ith leaf

References

  1. Abe M., Kobayashi Y., Yamamoto S., Daimon Y., Yamaguchi A., Ikeda Y., Ichinoki H., Notaguchi M., Goto K., Araki T. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science. 2005;309:1052–1056. doi: 10.1126/science.1115983. [DOI] [PubMed] [Google Scholar]
  2. Cannell M.G.R., Thornley J.H.M. Modelling components of plant respiration: some guising principles. Annals of Botany. 2000;85:45–54. doi: 10.1006/anbo.1999.0996. [DOI] [Google Scholar]
  3. Causton D.R., Venus J.C. The Biometry Of Plant Growth. London: Edward Arnold; 1981. [Google Scholar]
  4. Cho A. Life’s Patterns: No Need to Spell It Out? Science. 2004;303:782–783. doi: 10.1126/science.303.5659.782. [DOI] [PubMed] [Google Scholar]
  5. Falster D.S. (2003). http://www.bio.mq.edu.au/ecology/SMATR.
  6. Felsenstein J. PHYLIP-Phylogeny Inference Package (Version 3.2) Cladistics. 1989;5:164–166. [Google Scholar]
  7. Felsenstein J. PHYLIP-Phylogeny Inference Package (version 3.6). Distributed by the author. Seattle: Department of Genome Sciences, University of Washington; 2004. [Google Scholar]
  8. Franco M., Kelly C.K. The inter-specific mass-density relationship and plant geometry. Proc. Natl. Acad. Sci., (USA) 1998;95:7830–7835. doi: 10.1073/pnas.95.13.7830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Glass, Karopka T., Wolkenhauer O. Bioinformatics and The Virtual Cell (Bioinformatik und die Virtuelle Zelle) InformationTechnology. 2006;48:44–51. [Google Scholar]
  10. Gillete M.U., Sejnowski T.J. Biological clocks coordinately keep life on time. Science. 2005;309:1196–1198. doi: 10.1126/science.1111420. [DOI] [PubMed] [Google Scholar]
  11. Hoagland D, Arnon D. (1950). The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347.
  12. Jacobs W.P., Bullwinkel B. Compensatory growth in coleus shoots. American Journal of Botany. 1953;40:385–392. doi: 10.2307/2438521. [DOI] [Google Scholar]
  13. Jacobs W.P., Suthers H.B. Effect of leaf excision on flowering of Xanthium apical buds in culture under inductive and noninductive photoperiods. American Journal of Botany. 1974;61:1016–1020. doi: 10.2307/2441992. [DOI] [Google Scholar]
  14. Klingenberg C.P. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews. 1998;79:79–123. doi: 10.1017/S000632319800512X. [DOI] [PubMed] [Google Scholar]
  15. Mathai J.C., Sauna Z.E., John O., Sitaramam V. Rate limiting step in electron transport: osmotically sensitive diffusion of quinones through voids in the bilayer. Journal of Biological Chemistry. 1993;268:15442–15454. [PubMed] [Google Scholar]
  16. Meyerowitz E.M. Genetic Control of Cell Division Patterns in Developing Plants. Cell. 1997;88:299–308. doi: 10.1016/S0092-8674(00)81868-1. [DOI] [PubMed] [Google Scholar]
  17. Milner M., Patwardhan V., Bansode A., Nevagi S.A., Kulkarni S., Kamakaka R., Modak S.P. Constructing 3-D phylogenetic trees. Current Science. 2003;85:1471–1478. [Google Scholar]
  18. Newell A.C., Shipman P.D. Plants and Fibonacci. Journal of Statistical Physics. 2005;121:937–968. doi: 10.1007/s10955-005-8665-7. [DOI] [Google Scholar]
  19. Niklas K.J., Enquist B.J. Invariant scaling relationships for interspecific biomass production rates and body size. Proc. Natl. Acad. Sci., (USA) 2001;98:2922–2927. doi: 10.1073/pnas.041590298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nishimura A., Ashikari M., Lin S., Takashi T., Angeles E.R., Yamamoto T., Matsuoka M. Isolation of a rice regeneration quantitative trait loci gene and its application to transformation systems. Proc. Natl. Acad. Sci., (USA) 2005;102:11940–11944. doi: 10.1073/pnas.0504220102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Okubo H. In: Growth Cycle and Dormancy in Plants. Viemont J.D., Crabbé J., editors. U.K.: CABI Publishing; 2000. pp. 1–22. [Google Scholar]
  22. Page R.D.M. TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the BioSciences. 1996;12:357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  23. Raven J.A. The Vacuole: Cost-benefit analysis. In: Leight R.A., Sanders D., editors. The Plant Vacuole. New York: Academic Press; 1997. pp. 59–82. [Google Scholar]
  24. Reiss M.J. The allometry of growth and reproduction. Cambridge: Cambridge University Press; 1989. [Google Scholar]
  25. Richards R.A. Selectable traits to increase crop photosynthesis and yield of grain crops. Journal of Experimental Botany. 2000;51:447–458. doi: 10.1093/jexbot/51.suppl_1.447. [DOI] [PubMed] [Google Scholar]
  26. Rosato A., Strandburg K.J., Prinz F., Swendsen R.H. Why the Brazil nuts are on top: size segregation of particulate matter by shaking. Physical Review Letters. 1987;58:1038–1040. doi: 10.1103/PhysRevLett.58.1038. [DOI] [PubMed] [Google Scholar]
  27. Rothstein E.C., Lucchesi P.A. Redox control of the cell cycle: a radical encounter. Antioxidants & redox signaling. 2005;7:701–703. doi: 10.1089/ars.2005.7.701. [DOI] [PubMed] [Google Scholar]
  28. Shipley B., Vu T.-T. Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytologist. 2002;153:359–365. doi: 10.1046/j.0028-646X.2001.00320.x. [DOI] [Google Scholar]
  29. Sitaramam V., Madhavarao C.N. The Energetic basis of Osmotolerance in plants: Physical principles. Journal of Theoretical Biology. 1997;189:333–352. doi: 10.1006/jtbi.1997.0522. [DOI] [PubMed] [Google Scholar]
  30. Slater M. Manometric methods and phosphate determination. Methods in Enzymology. 1967;10:19–29. doi: 10.1016/0076-6879(67)10006-2. [DOI] [Google Scholar]
  31. Smith B.N, Lytle C.M, Hansen L.D. (1995). Predicting plant gowth rates from dark respiration rates: an experimental approach. In: Proceedings: wildland shrub and arid land restoration symposium, Editors: Roundy B.A, McArthur E.D, Haley J.S, Mann D.K. 1993 October 19–21; Las Vegas, NV. Gen. Tech. Rep. INT-GTR=315. Ogden, UT: U.S. Department of agriculture, Forest Service, Intermountain research Station. http://www.fs.fed.us/rm/pubs/int_gtr315/4_smith.pdf.
  32. Sokal R.R., Rohlf F.J. Biometry: the principles and practice of statistics in biological research. 3. San Francisco: Freeman WH; 1995. [Google Scholar]
  33. West G.B., Savage V.M., Gillooly J., Enquist B.J., Woodruff W.H., Brown J.H. Why does metabolic rate scale with body size? and the subsequent correspondence. Nature. 2003;421:713–714. doi: 10.1038/421713a. [DOI] [PubMed] [Google Scholar]
  34. Yin X., Struik P.C., Kropff M.J. Role of crop physiology in predicting gene-to-phenotype relationships. Trends Plant Science. 2004;9:426–432. doi: 10.1016/j.tplants.2004.07.007. [DOI] [PubMed] [Google Scholar]

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