Circadian Rhythms and Heterosis

Most living organisms including plants and humans have adapted to 24-hour day-night cycles as a result of the Earth’s rotation. This adaptation involves constant coordination and balance between intrinsic circadian rhythms and extrinsic environmental cues such as light, temperature, food availability, and predatory pressure. Circadian rhythms were first recorded in sensitive heliotrope plants (probably Mimosa pudica L.) by Jean Jacques Ortous de Mairan, a French astronomer, in 1729. Carolus Linnaeus (1707-1778) was inspired to design an artistic living clock using the opening and closing of flowers on living plants to mark the hours, although they were never planted. Charles R. Darwin systematically measured and quantified leaf movements and published the results with his son in the book, The Power of Movement in Plants in 1880. The early work on leaf movements in plants has seeded the modern field of circadian biology. The food anticipatory and locomoter activities in rats were not investigated until 1920’s. Although extensive research of circadian rhythms emerges late in humans, the study of metabolic balances and physiological and pathological traits dates back to the work of Santorio Sanctorius (1561-1636), who recorded daily body weight changes over many years in response to intake of food and nutrition and releases through emunctories and perspiration. These botanical and physiological experiments have founded the modern field of chronobiology, linking circadian rhythms with metabolism, physiology, growth vigor, disease, and human health.

The Arabidopsis thaliana clock consists of a central loop and two peripheral (morning and evening) loops. The central loop includes transcription factors CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), LATE ELONGATED HYPOCOTYL (LHY), CCA1 HIKING EXPEDITION (CHE), and TIMING OF CAB EXPRESSION 1 (TOC1). TOC1 positively regulates expression of CCA1 and LHY that have redundant but non-overlapping functions, while CCA1 and LHY bind to the promoter of TOC1 and inhibit its expression. CHE interacts with TOC1 and binds to CCA1 promoter and promotes its expression, whereas CCA1 and LHY repress CHE expression. In A. thaliana, circadian regulators affect rhythms and period of the clock as well as its input and output pathways. At least ~10% of genes, including those involved in photosynthesis and starch metabolism, and up to 90% of transcriptome are affected by the circadian rhythms. Moreover, day-length and circadian effects on transitory starch metabolism correlate with diurnal expression of these metabolic genes. Hence, maintaining circadian regulation increases CO2 fixation and growth, whereas disrupting circadian rhythms reduces fitness. Using Arabidopsis hybrids and allopolyploids as experimental systems, we are testing how and why circadian rhythms are altered to promote growth vigor and improve fitness.

Wikipedia about Circadian Rhythms

Ten selected papers about circadian rhythms and metabolism

  1. Bass J, Takahashi JS: Circadian integration of metabolism and energetics. Science 330: 1349-54 (2010).
  2. Darwin CR, Darwin F: The Power of Movement in Plants. John Murray, London (1880).
  3. de Montaigu A, Toth R, Coupland G: Plant development goes like clockwork. Trends Genet 26: 296-306 (2010).
  4. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA: Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-3 (2005).
  5. Harmer SL: The circadian system in higher plants. Annu Rev Plant Biol 60: 357-77 (2009).
  6. McClung CR: Plant circadian rhythms. Plant Cell 18: 792-803 (2006).
  7. Millar AJ, Short SR, Chua NH, Kay SA: A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell 4: 1075-87 (1992).
  8. Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ: Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457: 327-31 (2009).
  9. Pruneda-Paz JL, Kay SA: An expanding universe of circadian networks in higher plants. Trends Plant Sci 15: 259-65 (2010).
  10. Wijnen H, Young MW: Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet 40: 409-48 (2006).