RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 37, 2016, Pages 10424-10429

  Suetsugu, Noriyuki ^a,b   Takemiya, Atsushi ^a,c   Kong, Sam Geun ^a,d   Higa, Takeshi ^a,e   Komatsu, Aino ^b   Shimazaki, Ken Ichiro ^a   Kohchi, Takayuki ^b   Wada, Masamitsu ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c YAMAGUCHI UNIVERSITY   (Japan)

^d Kongju National University   (South Korea)

^e TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

Arabidopsis; Blue light; Chloroplast movement; Marchantia; Phototropin

Indexed keywords

BLUE LIGHT SIGNALING 1 KINASE; CARRIER PROTEINS AND BINDING PROTEINS; NONPHOTOTROPIC HYPOCOTYL 3; NRL PROTEIN FOR CHLOROPLAST MOVEMENT 1; PHOSPHOTRANSFERASE; PHOTOTROPIN; ROOT PHOTOTROPISM 2; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; NPH1 PROTEIN, ARABIDOPSIS; NPH3 PROTEIN, ARABIDOPSIS; PHOSPHOPROTEIN; PHOT2 PROTEIN, ARABIDOPSIS; RPT2 PROTEIN, ARABIDOPSIS;

BLUE LIGHT; CHLOROPLAST; CONFERENCE PAPER; EMBRYOPHYTA; HYPOCOTYL; MARCHANTIA; MOLECULAR SIZE; NONHUMAN; PHOTOTROPISM; PLANT EVOLUTION; PLANT GENOME; PLANT LEAF; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRIDIPLANTAE; ARABIDOPSIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PHOTOSYNTHESIS; PLANT ROOT; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; EMBRYOPHYTA; LIGHT; PHOSPHOPROTEINS; PHOTOSYNTHESIS; PHOTOTROPISM; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED;

EID: 84987681554     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1602151113     Document Type: Article

References (60)

1. Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21-45.
2. Bögre L, Okrész L, Henriques R, Anthony RG (2003) Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 8(9):424-431.
3. Suetsugu N, Wada M (2013) Evolution of three LOV blue light receptor families in green plants and photosynthetic stramenopiles: Phototropin, ZTL/FKF1/LKP2 and aureochrome. Plant Cell Physiol 54(1):8-23.
4. Sakai T, et al. (2001) Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98(12): 6969-6974.
5. Kinoshita T, et al. (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414(6864):656-660.
6. Inoue S, Kinoshita T, Takemiya A, Doi M, Shimazaki K (2008) Leaf positioning of Arabidopsis in response to blue light. Mol Plant 1(1):15-26.
7. Kagawa T, et al. (2001) Arabidopsis NPL1: A phototropin homolog controlling the chloroplast high-light avoidance response. Science 291(5511):2138-2141.
8. Jarillo JA, et al. (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410(6831):952-954.
9. Kozuka T, Kong SG, Doi M, Shimazaki K, Nagatani A (2011) Tissue-autonomous promotion of palisade cell development by phototropin 2 in Arabidopsis. Plant Cell 23(10):3684-3695.
10. Motchoulski A, Liscum E (1999) Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science 286(5441):961-964.
11. Sakai T, Wada T, Ishiguro S, Okada K (2000) RPT2. A signal transducer of the phototropic response in Arabidopsis. Plant Cell 12(2):225-236.
12. Gingerich DJ, Hanada K, Shiu SH, Vierstra RD (2007) Large-scale, lineage-specific expansion of a bric-a-brac/tramtrack/broad complex ubiquitin-ligase gene family in rice. Plant Cell 19(8):2329-2348.
13. Inada S, Ohgishi M, Mayama T, Okada K, Sakai T (2004) RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16(4):887-896.
14. Pedmale UV, Liscum E (2007) Regulation of phototropic signaling in Arabidopsis via phosphorylation state changes in the phototropin 1-interacting protein NPH3. J Biol Chem 282(27):19992-20001.
15. Tsuchida-Mayama T, et al. (2008) Mapping of the phosphorylation sites on the phototropic signal transducer, NPH3. Plant Sci 174(6):626-633.
16. Haga K, Tsuchida-Mayama T, Yamada M, Sakai T (2015) Arabidopsis ROOT PHOTOTROPISM2 contributes to the adaptation to high-intensity light in phototropic responses. Plant Cell 27(4):1098-1112.
17. de Carbonnel M, et al. (2010) The Arabidopsis PHYTOCHROME KINASE SUBSTRATE2 protein is a phototropin signaling element that regulates leaf flattening and leaf positioning. Plant Physiol 152(3):1391-1405.
18. Harada A, Takemiya A, Inoue S, Sakai T, Shimazaki K (2013) Role of RPT2 in leaf positioning and flattening and a possible inhibition of phot2 signaling by phot1. Plant Cell Physiol 54(1):36-47.
19. Kozuka T, Suetsugu N, Wada M, Nagatani A (2013) Antagonistic regulation of leaf flattening by phytochrome B and phototropin in Arabidopsis thaliana. Plant Cell Physiol 54(1):69-79.
20. Tsutsumi T, Takemiya A, Harada A, Shimazaki K (2013) Disruption of ROOT PHOTOTROPISM2 gene does not affect phototropin-mediated stomatal opening. Plant Sci 201-202:93-97.
21. Wan Y, et al. (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24(2):551-565.
22. Lariguet P, et al. (2006) PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism. Proc Natl Acad Sci USA 103(26):10134-10139.
23. Demarsy E, et al. (2012) Phytochrome kinase substrate 4 is phosphorylated by the phototropin 1 photoreceptor. EMBO J 31(16):3457-3467.
24. Suetsugu N, Wada M (2016) Evolution of the cp-actin-based motility system of chloroplasts in green plants. Front Plant Sci 7:561.
25. Kagawa T, Kasahara M, Abe T, Yoshida S, Wada M (2004) Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. Plant Cell Physiol 45(4):416-426.
26. Kasahara M, Kagawa T, Sato Y, Kiyosue T, Wada M (2004) Phototropins mediate blue and red light-induced chloroplast movements in Physcomitrella patens. Plant Physiol 135(3):1388-1397.
27. Komatsu A, et al. (2014) Phototropin encoded by a single-copy gene mediates chloroplast photorelocation movements in the liverwort Marchantia polymorpha. Plant Physiol 166(1):411-427.
28. Zhang L, Du L, Shen C, Yang Y, Poovaiah BW (2014) Regulation of plant immunity through ubiquitin-mediated modulation of Ca2+ -calmodulin-AtSR1/CAMTA3 signaling. Plant J 78(2):269-281.
29. Furutani M, et al. (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134(21):3849-3859.
30. Takemiya A, et al. (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun 4:2094.
31. Wada M, Kong SG (2011) Analysis of chloroplast movement and relocation in Arabidopsis. Methods Mol Biol 774:87-102.
32. Ishizaki K, Johzuka-Hisatomi Y, Ishida S, Iida S, Kohchi T (2013) Homologous recombination-mediated gene targeting in the liverwort Marchantia polymorpha L. Sci Rep 3:1532.
33. Barbosa ICR, Schwechheimer C (2014) Dynamic control of auxin transport-dependent growth by AGCVIII protein kinases. Curr Opin Plant Biol 22:108-115.
34. Cheng Y, Qin G, Dai X, Zhao Y (2007) NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis. Proc Natl Acad Sci USA 104(47): 18825-18829.
35. Cheng Y, Qin G, Dai X, Zhao Y (2008) NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis. Proc Natl Acad Sci USA 105(52):21017-21022.
36. Li Y, Dai X, Cheng Y, Zhao Y (2011) NPY genes play an essential role in root gravitropic responses in Arabidopsis. Mol Plant 4(1):171-179.
37. Furutani M, Nakano Y, Tasaka M (2014) MAB4-induced auxin sink generates local auxin gradients in Arabidopsis organ formation. Proc Natl Acad Sci USA 111(3): 1198-1203.
38. Harper RM, et al. (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12(5):757-770.
39. Aida M, Vernoux T, Furutani M, Traas J, Tasaka M (2002) Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129(17):3965-3974.
40. Wada M (1988) Chloroplast photoorientation in enucleated fern protonemata. Plant Cell Physiol 29(7):1227-1232.
41. Suetsugu N, Kagawa T, Wada M (2005) An auxilin-like J-domain protein, JAC1, regulates phototropin-mediated chloroplast movement in Arabidopsis. Plant Physiol 139(1):151-162.
42. Kodama Y, Suetsugu N, Kong SG, Wada M (2010) Two interacting coiled-coil proteins, WEB1 and PMI2, maintain the chloroplast photorelocation movement velocity in Arabidopsis. Proc Natl Acad Sci USA 107(45):19591-19596.
43. Usami H, et al. (2012) CHUP1 mediates actin-based light-induced chloroplast avoidance movement in the moss Physcomitrella patens. Planta 236(6):1889-1897.
44. Suetsugu N, et al. (2012) The KAC family of kinesin-like proteins is essential for the association of chloroplasts with the plasma membrane in land plants. Plant Cell Physiol 53(11):1854-1865.
45. Oikawa K, et al. (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15(12):2805-2815.
46. Suetsugu N, et al. (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107(19):8860-8865.
47. Ichikawa S, Yamada N, Suetsugu N, Wada M, Kadota A (2011) Red light, phot1 and JAC1 modulate phot2-dependent reorganization of chloroplast actin filaments and chloroplast avoidance movement. Plant Cell Physiol 52(8):1422-1432.
48. Rosso MG, et al. (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53(1-2): 247-259.
49. Huala E, et al. (1997) Arabidopsis NPH1: A protein kinase with a putative redoxsensing domain. Science 278(5346):2120-2123.
50. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
51. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754-755.
52. Suetsugu N, Higa T, Kong SG, Wada M (2015) PLASTID MOVEMENT IMPAIRED1 and PLASTID MOVEMENT IMPAIRED1-RELATED 1 mediate photorelocation movements of both chloroplasts and nuclei. Plant Physiol 169(2):1155-1167.
53. Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25(6):989-994.
54. Suetsugu N, Kong SG, Kasahara M, Wada M (2013) Both LOV1 and LOV2 domains of phototropin2 function as the photosensory domain for hypocotyl phototropic responses in Arabidopsis thaliana (Brassicaceae). Am J Bot 100(1):60-69.
55. Ueno K, Kinoshita T, Inoue S, Emi T, Shimazaki K (2005) Biochemical characterization of plasma membrane H+ -ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant Cell Physiol 46(6):955-963.
56. Takemiya A, Yamauchi S, Yano T, Ariyoshi C, Shimazaki K (2013) Identification of a regulatory subunit of protein phosphatase 1 which mediates blue light signaling for stomatal opening. Plant Cell Physiol 54(1):24-35.
57. Kinoshita T, Shimazaki Ki (1999) Blue light activates the plasma membrane H(+ )-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18(20): 5548-5558.
58. Kong SG, Arai Y, Suetsugu N, Yanagida T, Wada M (2013) Rapid severing and motility of chloroplast-actin filaments are required for the chloroplast avoidance response in Arabidopsis. Plant Cell 25(2):572-590.
59. Ishizaki K, et al. (2015) Development of gateway binary vector series with four different selection markers for the liverwort Marchantia polymorpha. PLoS One 10(9): e0138876.
60. Kubota A, Ishizaki K, Hosaka M, Kohchi T (2013) Efficient Agrobacterium-mediated transformation of the liverwort Marchantia polymorpha using regenerating thalli. Biosci Biotechnol Biochem 77(1):167-172.