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

The role of phytochrome C in gravitropism and phototropism in Arabidopsis thaliana

Prem Kumar A B , Crystal E. Montgomery A B and John Z. Kiss A C
+ Author Affiliations
- Author Affiliations

A Department of Botany, Miami University, Oxford, OH 45056, USA.

B These two authors contributed equally to this work.

C Corresponding author. Email: kissjz@muohio.edu

Functional Plant Biology 35(4) 298-305 https://doi.org/10.1071/FP08013
Submitted: 19 January 2008  Accepted: 10 April 2008   Published: 3 June 2008

Abstract

The phytochrome (phy) photoreceptors, which consist of a small gene family PHYA-E in dicot plants, play important roles in regulating many light-induced responses in plants. Although the best characterised phytochromes are phytochrome A (phyA) and phytochrome (phyB), the functions of phyD and phyE have been increasingly studied. Phytochrome C (phy C) has been the most poorly understood member of the photoreceptor family, since isolation of phyC mutants only has been accomplished within the last few years. Recent reports show that phyC functions in hypocotyl elongation, rosette leaf morphology, and timing of flowering. In the present study, we show that phyC plays a role in tropisms in seedlings and inflorescence stems of light-grown Arabidopsis thaliana (L.) Heynh. (Wassilewskija ecotype). Phytochrome C has a positive effect on gravitropism in hypocotyls and stems, but it has a limited role in root gravitropism. In contrast, phyC attenuates the positive phototropic response to blue light in hypocotyls and the red-light-based positive phototropism in roots. Phytochrome D (phy D) also mediates gravitropism in hypocotyls and inflorescence stems and attenuates positive phototropism in response to blue in hypocotyls and stems. Thus, phyC can be added to the list of the other four phytochromes, which play various roles in both gravitropism and phototropism in plant organs. This report also supports the growing body of evidence demonstrating cross talk between phytochromes and blue-light photoreceptors.

Additional keywords: Arabidopsis, gravitropism, phototropism, phytochrome C.


Acknowledgements

Financial support was provided by the National Aeronautics and Space Administration (NASA) through grant NCC2–1200.


References


Aukerman MJ, Hirschfeld M, Wester L, Weaver M, Clack T, Amasino RM, Sharrock RA (1997) A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. The Plant Cell 9, 1317–1326.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Balasubramanian S, Sureshkumar S, Agrawal M, Michael TP, Wessinger C, Maloof JN, Clark R, Warthmann N, Chory J, Weigel D (2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana. Nature Genetics 38, 711–715.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends in Plant Science 7, 204–210.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cashmore AR (2003) Cryptochromes: enabling plants and animals to determine circadian time. Cell 114, 537–543.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cho H-Y, Tseng T-S, Kaiserli E, Sullivan S, Christie JM, Briggs WR (2007) Physiological roles of the light, oxygen, or voltage domains of phototropin 1 and phototropin 2 in Arabidopsis. Plant Physiology 143, 517–529.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Correll MJ, Kiss JZ (2002) Interactions between gravitropism and phototropism in plants. Journal of Plant Growth Regulation 21, 89–101.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Correll MJ, Kiss JZ (2005) The roles of phytochromes in elongation and gravitropism of roots. Plant & Cell Physiology 46, 317–323.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Correll MJ, Coveney KM, Raines SV, Mullen JL, Hangarter RP, Kiss JZ (2003) Phytochromes play a role in phototropism and gravitropism in Arabidopsis roots. Advances in Space Research 31, 2203–2210.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

DeBlasio SL, Mullen JL, Luesse DR, Hangarter RP (2003) Phytochrome modulation of blue light-induced chloroplast movements in Arabidopsis. Plant Physiology 133, 1471–1479.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Endo M, Mochizuki N, Suzuki T, Nagatani A (2007) CRYPTOCHROME2 in vascular bundles regulates flowering in Arabidopsis. The Plant Cell 19, 84–93.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fitzelle KJ, Kiss JZ (2001) Restoration of gravitropic sensitivity in starch-deficient mutants of Arabidopsis by hypergravity. Journal of Experimental Botany 52, 265–275.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franklin KA, Davis SJ, Stoddart WM, Vierstra RD, Whitelam GC (2003) Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. The Plant Cell 15, 1981–1989.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franklin KA, Larner VS, Whitelam GC (2005) The signal transducing photoreceptors of plants. International Journal of Developmental Biology 49, 653–666.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hangarter RP (1997) Gravity, light and plant form. Plant, Cell & Environment 20, 796–800.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Janoudi A-K, Poff KL (1997) Multiple phytochromes are involved in red light-induced enhancement of first positive curvature in Arabidopsis thaliana. Plant Physiology 113, 975–979.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kiss JZ, Guisinger MM, Miller AJ, Stackhouse KS (1997) Reduced gravitropism in hypocotyls of starch-deficient mutants of Arabidopsis. Plant & Cell Physiology 38, 518–525.
PubMed |
open url image1

Kiss JZ, Miller KM, Ogden LA, Roth KK (2002) Phototropism and gravitropism in lateral roots of Arabidopsis. Plant & Cell Physiology 43, 35–43.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kiss JZ, Mullen JL, Correll MJ, Hangarter RP (2003) Phytochromes A and B mediate red-light-induced positive phototropism in roots. Plant Physiology 131, 1411–1417.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kumar P, Kiss JZ (2006) Modulation of phototropism by phytochrome E and attenuation of gravitropism by phytochromes B and E in inflorescence stems. Physiologia Plantarum 127, 304–311.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lariguet P, Fankhauser C (2004) Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. The Plant Journal 40, 826–834.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Li B, Suzuki J-I, Hara T (1998) Latitudinal variation in plant size and relative growth rate in Arabidopsis thaliana. Oecologia 115, 293–301.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lu Y-T, Feldman LJ (1997) Light-regulated root gravitropism: a role for, and characterization of, a calcium/calmodulin-dependent protein kinase homolog. Planta 203, S91–S97.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Más P, Devlin PF, Panda S, Kay SA (2000) Functional interaction of phytochrome B and cryptochrome 2. Nature 408, 207–211.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Molas ML , Kiss JZ (2008) PKS1 plays a role in red-light-based positive phototropism in roots. Plant, Cell & Environment 31, (In press).

Møller SG, Ingles PJ, Whitelam GC (2002) The cell biology of phytochrome signalling. The New Phytologist 54, 553–590. open url image1

Monte E, Alonso JM, Eker JR, Zhang Y, Li X, Young J, Austin-Phillips S, Quail PH (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. The Plant Cell 15, 1962–1980.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mullen JL, Ishikawa H, Evans ML (1998) Analysis of changes in relative elemental growth patterns in the elongation zone of Arabidopsis roots upon gravistimulation. Planta 206, 598–603.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mullen JL, Wolverton C, Ishikawa H, Evans ML (2000) Kinetics of constant gravitropic stimulus responses in Arabidopsis roots using a feedback system. Plant Physiology 123, 665–670.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Parks BM, Spalding EP (1999) Sequential and coordinated action of phytochromes A and B during Arabidopsis stem growth revealed by kinetic analysis. Proceedings of the National Academy of Sciences USA 96, 14142–14146.
Crossref | GoogleScholarGoogle Scholar | open url image1

Parks BM, Quail PH, Hangarter RP (1996) Phytochrome A regulates the induction of phototropic enhancement in Arabidopsis thaliana. Plant Physiology 110, 155–162.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Poppe C, Hangarter RP, Sharrock RA, Nagy F, Schäfer E (1996) The light-induced reduction of the gravitropic growth-orientation of seedlings of Arabidopsis thaliana (L.) Heynh is a photomorphogenic response mediated synergistically by the far-red-absorbing forms of phytochromes A and B. Planta 199, 511–514.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Qin M, Kuhn R, Moran S, Quail PH (1997) Overexpressed phytochrome C has similar photosensory specificity to phytochrome B but a distinctive capacity to enhance primary leaf expansion. The Plant Journal 12, 1163–1172.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Quail PH (2002) Phytochrome photosensory signalling networks. Nature Reviews. Molecular Cell Biology 3, 85–93.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Robson PRH, Smith H (1996) Genetic and transgenic evidence that phytochromes A and B act to modulate the gravitropic orientation of Arabidopsis thaliana hypocotyls. Plant Physiology 110, 211–216.
PubMed |
open url image1

Ruppel NJ, Hangarter RP, Kiss JZ (2001) Red-light-induced positive phototropism in Arabidopsis roots. Planta 212, 424–430.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sakai T, Wada T, Ishiguro S, Okada K (2000) RPT2: a signal transducer of the phototropic response in Arabidopsis. The Plant Cell 12, 225–236.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schepens I, Duek P, Fankhauser C (2004) Phytochrome-mediated light signalling in Arabidopsis. Current Opinion in Plant Biology 7, 564–569.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Whippo CW, Hangarter RP (2003) Second positive phototropism results from coordinated co-action of the phototropins and cryptochromes. Plant Physiology 132, 1499–1507.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Whippo CW, Hangarter RP (2004) Phytochrome modulation of blue-light-induced phototropism. Plant, Cell & Environment 27, 1223–1228.
Crossref | GoogleScholarGoogle Scholar | open url image1