摘要
花青素和叶绿素是高等植物中存在的两大类非常重要的色素。花青素存在于植物表皮细胞的液泡中,使高等植物的花、果实、种皮呈现出红、蓝、紫的颜色,花青素在植物中行使着多种重要的生理功能,例如吸引授粉者和种子传播者,保护植物免受昆虫攻击、缓解UV-B辐射以及具有很强的抗氧化活性等。近年的研究表明,花青素的摄入还能够降低人类心血管疾病、糖尿病、关节炎和癌症的发病率;而叶绿素则是高等植物中最为重要的一类色素,它不仅是绿色植物的主要色素,更是植物进行光合作用的重要物质,同时叶绿素在人类的日常生活中也占有非常重要的作用,具有造血、解毒、降低胆固醇以及抗突变的保健功效。因此,对于花青素以及叶绿素的合成代谢及其调控机制的深入研究,对于人类的保健以及增加作物产量都具有非常重要的意义。细胞分裂素作为一类重要的植物激素在植物生长发育的整个过程中起到了非常重要的作用,包括调节植物细胞的分裂以及新陈代谢,诱导叶绿体的发育,调节植物地上部分以及根系的发育,延缓叶片衰老等。本文以模式植物拟南芥为材料,采用生理分析和分子生物学方法研究了细胞分裂素对植物花青素和叶绿素含量的影响,以及红光受体PHYB及光敏色素相互作用因子(Phytochrome-interacting factors, PIFs)在此过程中的调控作用。研究结果表明:
(1)光下外源细胞分裂素(6-BA)可诱导拟南芥幼苗中花青素的大量积累,花青素含量随着处理浓度及处理时间的增加而增加,并且花青素合成通路中的三个重要酶,查尔酮合酶(CHS)、查尔酮异构酶(CHI)及二氢黄酮醇-4-还原酶(DFR)的基因表达量明显受到了外源细胞分裂素的上调,说明外源6-BA通过诱导花青素合成基因表达量的增加,从而促进花青素的积累;
(2)光下外源6-BA可以显著降低拟南芥幼苗新生叶片中叶绿素的含量,且这种降低没有浓度依赖性,0.1“M6-BA处理效果最为明显;
(3)拟南芥中存在三种细胞分裂素受体:AHK2、AHK3和AHK4/CRE1,光下6-BA对拟南芥幼苗花青素以及叶绿素含量的影响主要是通过其受体AHK3与CRE1实现的:
(4)6-BA对拟南芥幼苗花青素以及叶绿素含量的影响依赖于光照,并且受红光信号的调控。光下外源6-BA处理下,红光受体PHYB突变体phyB幼苗中花青素积累量明显减少,并且新生叶片中叶绿素的含量变化也较小,phyB中花青素合成基因的表达量明显较野生型低,说明PHYB信号参与调节了光下6-BA对拟南芥幼苗花青素以及叶绿素含量的影响;
(5)本研究证明PIFs家族中的PIF4在光下6-BA诱导的拟南芥幼苗花青素及叶绿素含量变化中起到了负调控的作用。光下外源6-BA处理下,对照Col-0、突变体pifl、pif3、pif4、pif5及其过表达系PIF3OX和PIF5OX幼苗中均积累了大量的花青素,并且新生叶片中叶绿素含量也显著下降,但是过表达系PIF4OX中花青素积累量明显较对照少,并且新生叶片中叶绿素的含量变化也较小。另外,PIF4OX幼苗中花青素合成基因的表达量明显较Col-0、 PIF3OK及PIF5OX (?)(?),进一步证明PIF4在6-BA诱导的拟南芥幼苗花青素及叶绿素含量变化中起到的负调控作用。
Anthocyanins and chlorophyll are two classes of very important pigments in higher plants. Anthocyanins are the pigments in vacuole of epidermal cell. They have caused the red, blue or purple colour in flowers, fruits and seed coats. Anthocyanins are provided with various important physiological functions in plants. For example, it appeals to pollinators and seed dispersers, defends protects plant against insect attracting and relieves the damage of UV-B radiation, as well as acts as powerful antioxidants etc. Recent studies show that anthocyanins could reduce the incidence of human cardiovascular disease, diabetes, arthritis and cancer. Chlorophyll is an extremely important kind of pigment in higher plants. It is not only an important pigment, but also the critical substance in photosynthesis of plant. Meanwhile, chlorophyll also occupies a very important role in human daily life. It is provided with good effects on hemopoiesis, detoxification, reduce cholesterol level and anti-mutation. Therefore, the further study on the synthesis metabolism of anthocyanins and chlorophyll and its regulation mechanism is essential to human health and increase in crop production. Cytokinins as a kind of phytohormones play critical roles in plant growth and development, including regulation of cell division and metabolism, stimulation chloroplast development, modulation of shoot and root development, and delay of leaf senescence in plants etc. In the present study, the model plant Arabidopsis thaliana was used as material, the effects of cytokinins on anthocyanin and chlorophyll content, and the regulatory role of red light receptor PHYB and PIFs (Phytochrome-interacting factors) in this process were investigated by physiological and molecular biology method. The results showed that:
(1) In light, the marked accumulation of anthocyanins Arabidopsis thaliana seedlings was induce by treatment with exogenous cytokinin (6-benzyladenine,6-BA). Levels of mRNAs for three genes of the anthocyanin biosynthesis pathway, chalcone synthase (CHS), chalcone isomerase (CHI), and dihydroflavonol reductase (DFR) were obviously up-regulated by exogenous6-BA. These data suggested that exogenous6-BA promoted anthocyanins accumulation by inducing the expression of anthocyanin synthesis genes.
(2) Chlorophyll content in newborn leaves of Arabidopsis thaliana was significantly decreased by6-BA in light. The decrease of chlorophyll content was not concentration-dependent manner. The treatment of0.1μM6-BA showed the maximum efficiency.
(3) In Arabidopsis thaliana, there is three cytokinin receptors, AHK2(Arabidopsis his kinase2), AHK3and AHK4/CRE1. We found that AHK3and CRE1played an important role in the changes of anthocyanin and chlorophyll content induced by6-BA in light.
(4) Effects of6-BA on anthocyanin and chlorophyll content were dependent on light and regulated by red light signal. The anthocyanin accumulation content in red light photoreceptor PHYB mutant seedlings was marked decrease and the change of chlorophyll content in newborn leaves of it was also less than that of the control in the exogenous6-BA treatment under light. The expression levels of three genes of anthocyanin biosynthesis pathway in phyB were much less than that of control (Col-0) in the exogenous6-BA treatment under light. These results indicated that PHYB signal was involved in regulating the effects of cytokinins on the changes of anthocyanin and chlorophyll content in Arabidopsis seedlings under light.
(5) Our data indicated that PIF4negatively regulated the changes of anthocyanin and chlorophyll contents induced by6-BA. In6-BA treatments, the anthocyanin in control (Col-0), mutants (pif1, pif3, pif4, pif5) and over-expression line (PIF3OX and PIF5OX) seedlings obviously accumulated, and the chlorophyll contents in the newborn leaves of them were also marked decrease. But the anthocyanin accumulation content in PIF4OX seedlings was much smaller than that of in control in6-BA treatment. So was in changes of cholorphyll content in newborn leaves of it. Others, the expression levels of anthocyanin biosynthesis genes in PIF3OX and PIF5OX seedlings were much less than that of Col-0, PIF3OX and PIF5OX in6-BA treatment. The present data indicated that PIF4in Arabidopsis seedlings was the essential role in the changes of anthocyanin and chlorophyll contents induced by6-BA.
引文
Abidi, F., Girault. T.. Douillet. O., Guillemain, G.. Sintes, G., Laffaire, M., Ahmed, H.B., Smiti, S., Huch6-Thelier, L., Leduc, N.,2013. Blue light effects on rose photosynthesis and photomorphogenesis. Plant Biology 15.67-74.
Ahmad, M., Cashmore, A.R.,1993. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor.
Ahmad, M., Cashmore, A.R.,1997. The blue-light receptor cryptochrome 1 shows functional dependence on phytochrome A or phytochrome B in Arabidopsis thaliana. The Plant Journal 11.421-427.
Al-Sady, B., Kikis, E.A., Monte, E., Quail, P.H.,2008. Mechanistic duality of transcription factor function in phytochrome signaling. Proceedings of the National Academy of Sciences 105, 2232-2237.
Alan. R., 1994. The spectral determination of chlorophyll a and b. as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Plant Physiol 144,307-313.
Arabidopsis. G.I.,2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408,796.
Argueso, C.T., Ferreira. F.J., Kieber. J.J.,2009. Environmental perception avenues:the interaction of cytokinin and environmental response pathways. Plant, Cell & Environment 32,1147-1160.
Arnon, D.I.,1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24,1.
Ashikari. M., Sakakibara. H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano. H., Matsuoka, M.,2005. Cytokinin oxidase regulates rice grain production. Science 309,741-745.
Babiker. A.G.T.. Butler, L.G., Ejeta, G., Woodson, W.R.,1993. Enhancement of ethylene biosynthesis and germination by cytokinins and 1-aminocyclopropane-1-carboxylic acid in Striga asiatica seeds. Physiologia Plantarum 89,21-26.
Bartrina, I., Otto, E.. Strnad, M., Werner, T.. Schmulling, T.,2011. Cytokinin Regulates the Activity of Reproductive Meristems, Flower Organ Size, Ovule Formation, and Thus Seed Yield in Arabidopsis thaliana. The Plant Cell 23,69-80.
Briggs, W.. Beck, C., Cashmore. A., Christie. J., Hughes, J.. Jarillo, J., Kagawa, T., Kanegae, H., Liscum. E.. Nagatani. A.,2001. The phototropin family of photoreceptors. The Plant Cell Online 13.993-997.
Briggs. W.R., Huala, E.,1999. Blue-light photoreceptors in higher plants. Annual review of cell and developmental biology 15.33-62.
Briggs, W.R., Olney. M.A.,2001. Photoreceptors in plant photomorphogenesis to date. Five phytochromes. two cryptochromes, one phototropin. and one superchrome. Plant Physiology 125.85-88.
Brouillard. R., Chassaing. S., lsorez. G., Kueny-Stotz, M., Figueiredo, P.,2010. The visible flavonoids or anthocyanins:from research to applications. Recent advances on polyphenol research 2, 1-22.
Brown, B.A., Cloix. C., Jiang, G.H., Kaiserli, E., Herzyk, P., Kliebenstein, D.J., Jenkins, G.I.,2005. A UV-B-specific signaling component orchestrates plant UV protection. Proceedings of the National Academy of Sciences of the United States of America 102,18225-18230.
Cashmore, A.R., Jarillo, J.A., Wu, Y.-J., Liu, D.,1999. Cryptochromes:blue light receptors for plants and animals. Science 284,760-765.
Chagne,D., Lin-Wang, K., Espley, R.V., Volz, R.K., How, N.M., Rouse, S., Brendolise, C., Carlisle, C.M., Kumar, S., De Silva, N.,2013. An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiology 161,225-239.
Chen, D.Q., Li. Z.Y., Pan, R.C., Wang, X.J.,2006. Anthocyanin accumulation mediated by blue light and cytokinin in Arabidopsis seedlings. Journal of Integrative Plant Biology 48,420-425.
Chen, M., Chory, J., Fankhauser, C.,2004. Light signal transduction in higher plants. Annu. Rev. Genet.38,87-117.
Choi. G., Yi, H., Lee. J., Kwon, Y.K., Soh, M.S., Shin, B., Luka, Z., Hahn, T.R., Song, P.S.,1999. Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401, 610-613.
Chory, J., Wu, D.,2001. Weaving the complex web of signal transduction. Plant Physiology 125, 77-80.
Christie, J.M.,2007. Phototropin blue-light receptors. Annu. Rev. Plant Biol.58,21-45.
Clark, S.E., 2001. Meristems:start your signaling. Current opinion in plant biology 4,28-32.
Cline, M., Wesse, T., Iwamura, H.,1997. Cytokinin/auxin control of apical dominance in Ipomoea nil. Plant and Cell Physiology 38,659-667.
Cloix, C., Jenkins. G.I.,2008. Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin. Molecular Plant 1,118-128.
D'Agostino, I.B., Deruere, J., Kieber, J.J.,2000. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiology 124,1706-1717.
Das, P.K., Shin. D.H., Choi. S.-B., Park, Y.-I.,2012. Sugar-hormone cross-talk in anthocyanin biosynthesis. Molecules and cells 34,501-507.
Daviere, J.-M., de Lucas, M., Prat, S.,2008. Transcriptional factor interaction:a central step in DELLA function. Current opinion in genetics & development 18,295-303.
Davies, P.J.,2010. The plant hormones:their nature, occurrence, and functions. Plant hormones. Springer, pp.1-15.
De Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E., Prat, S.,2008. A molecular framework for light and gibberellin control of cell elongation. Nature 451.480-484.
DeBlasio, S.L., Luesse, D.L., Hangarter, R.P.,2005. A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiology 139,101-114.
Dehesh, K., Franci, C., Parks, B.M., Seeley, K.A., Short, T.W., Tepperman, J.M., Quail. P.H.,1993. Arabidopsis HY8 locus encodes phytochrome A. The Plant Cell Online 5,1081-1088.
Demmig-Adams, B., Adams, W.W.,2002. Antioxidants in photosynthesis and human nutrition. Science 298,2149-2153.
Deng, X.W., Quail, P.H.,1999. Signalling in light-controlled development. Seminars in cell & developmental biology. Elsevier, pp.121-129.
Devasagayam, T., Tilak, J., Boloor, K., Sane, K., Ghaskadbi, S., Lele, R., 2004. Free radicals and antioxidants in human health:current status and future prospects. JAPI2004 52,794-804.
DianYi, S., ZhongXiang, L., WeiWei, J.,2009. Biosynthesis, catabolism and related signal regulations of plant chlorophyll. Hereditas (Beijing) 31,698-704.
Fankhauser, C.,2001. The phytochromes, a family of red/far-red absorbing photoreceptors. Journal of Biological Chemistry 276,11453-11456.
Fankhauser. C., Yeh, K.C., Clark, J., Zhang, H., Elich, T.D., Chory, J.,1999. PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284, 1539-1541.
Favory, J.-J., Stec, A., Gruber, H., Rizzini, L., Oravecz, A., Funk, M., Albert, A., Cloix, C., Jenkins, G.I., Oakeley, E.J.,2009. Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. The EMBO journal 28,591-601.
Franklin, K.A., Whitelam, G.C.,2004. Light signals, phytochromes and cross-talk with other environmental cues. Journal of Experimental Botany 55,271-276.
Fujimori, T., Yamashino, T., Kato, T., Mizuno, T.,2004. Circadian-controlled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana. Plant and Cell Physiology 45,1078-1086.
Fujita, A., Soma, N., Goto-Yamamoto. N., Shindo, H., Kakuta, T.. Koizumi. T.. Hashizume, K.,2005. Anthocyanidin reductase gene expression and accumulation of flavan-3-ols in grape berry. American journal of enology and viticulture 56,336-342.
Gallagher, S., Short, T.W., Ray, P.M., Pratt, L.H., Briggs, W.R.,1988. Light-mediated changes in two proteins found associated with plasma membrane fractions from pea stem sections. Proceedings of the National Academy of Sciences 85,8003-8007.
Genoud, T., Schweizer, F., Tscheuschler, A., Debrieux, D., Casal, J.J., Schafer, E., Hiltbrunner. A., Fankhauser, C., 2008. FHY1 mediates nuclear import of the light-activated phytochrome A photoreceptor. PLOS Genetics 4, e1000143.
Giron, D., Frago. E., Glevarec, G., Pieterse, C.M., Dicke, M.,2013. Cytokinins as key regulators in plant-microbe-insect interactions:connecting plant growth and defence. Functional Ecology.
Gollop, R., Even, S., Colova-Tsolova, V., Perl, A.,2002. Expression of the grape dihydroflavonol reductase gene and analysis of its promoter region. Journal of Experimental Botany 53, 1397-1409.
Grotewold. E., Sainz. M.B., Tagliani, L., Hernandez, J.M., Bowen, B., Chandler, V.L.,2000. Identification of the residues in the Myb domain of maize C1 that specify the interaction with the bHLH cofactor R. Proceedings of the National Academy of Sciences 97,13579-13584.
Guo, H., Mockler, T., Duong. H., Lin. C.,2001. SUB1, an Arabidopsis Ca2+-binding protein involved in cryptochrome and phytochrome coaction. Science 291,487-490.
Ha. S., Vankova. R., Yamaguchi-Shinozaki, K., Shinozaki. K., Tran, L.,2012. Cytokinins:metabolism and function in plant adaptation to environmental stresses. Trends in plant science 17,172.
Halliday. K.J., Hudson, M.,Ni, M., Qin, M., Quail, P.H.,1999. pocl:An Arabidopsis mutant perturbed in phytochrome signaling because of a T DNA insertion in the promoter of PIF3. a gene encoding a phytochrome-interacting bHLH protein. Proceedings of the National Academy of Sciences 96,5832-5837.
Harborne, J.B., Williams. C.A.,2000. Advances in flavonoid research since 1992. Phytochemistry 55. 481-504.
Higuchi. M., Pischke. M.S., Mahonen. A.P.. Miyawaki. K., Hashimoto, Y., Seki. M., Kobayashi. M., Shinozaki, K., Kato, T., Tabata, S.,2004. In planta functions of the Arabidopsis cytokinin receptor family. Proceedings of the National Academy of Sciences of the United States of America 101,8821-8826.
Hirose. N., Takei, K., Kuroha, T., Kamada-Nobusada, T.. Hayashi. H., Sakakibara, H.,2008. Regulation of cytokinin biosynthesis, compartmentalization and translocation. Journal of Experimental Botany 59,75-83.
Hisada, A., Hanzawa, H., Weller, J.L., Nagatani, A., Reid, J.B., Furuya, M.,2000. Light-induced nuclear translocation of endogenous pea phytochrome A visualized by immunocytochemical procedures. The Plant Cell Online 12,1063-1078.
Holton, T.A., Cornish, E.C.,1995. Genetics and biochemistry of anthocyanin biosynthesis. The Plant Cell 7,1071.
Hornitschek, P., Kohnen, M.V., Lorrain, S., Rougemont, J., Ljung, K., Lopez-Vidriero, I., Franco-Zorrilla, J.M., Solano, R., Trevisan, M., Pradervand, S.,2012. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. The Plant Journal.
Hornitschek, P., Lorrain, S., Zoetc, V., Michielin, O., Fankhauser, C.,2009. Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. The EMBO journal 28,3893-3902.
Hou. D.-X.,2003. Potential mechanisms of cancer chemoprevention by anthocyanins. Current molecular medicine 3.149-159.
Huang, Y.-J., Song, S., Allan, A.C., Liu, X.-F., Yin, X.-R., Xu, C.-J., Chen, K.,-S.,2013. Differential activation of anthocyanin biosynthesis in Arabidopsis and tobacco over-expressing an R2R3 MYB from Chinese bayberry. Plant Cell, Tissue and Organ Culture (PCTOC),491-499.
Hughes, J.,2013. Phytochrome Cytoplasmic Signaling. Annual review of plant biology 64.
Huq, F., Al-Sady. B.. Hudson. M., Kim. C., Apel, K., Quail, P.H.,2004. Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science Signaling 305,1937.
Huq, E., Kang, Y., Halliday, K.J., Qin, M., Quail, P.H.,2001. SRL1:a new locus specific to the phyB-signaling pathway in Arabidopsis. The Plant Journal 23,461-470.
Huq, E.. Quail, P.H.,2002. PIF4. a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. The EMBO journal 21,2441-2450.
Inoue, T., Higuchi, M., Hashimoto. Y., Seki. M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., Kakimoto. T.,2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409,1060-1063.
Jang. I.C., Henriques, R.. Seo. H.S.. Nagatani, A.. Chua. N.H.,2010. Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COPI E3 ligase in the nucleus. Plant Cell 22.2370-2383.
Kakimoto, T.,2001. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant and Cell Physiology 42.677-685.
Kaufmann. K., Pajoro, A., Angenent. G.C.,2010. Regulation of transcription in plants:mechanisms controlling developmental switches. Nature Reviews Genetics 11.830-842.
Khanna. R., Huq, E., Kikis, E.A., Al-Sady, B., Lanzatella. C. Quail. P.H.,2004. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. The Plant Cell Online 16.3033-3044.
Kircher, S., Kozma-Bognar, L.. Kim. L.. Adam, E.. Harter. K., Schafer. E.. Nagy, F.,1999. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. The Plant Cell Online 11,1445-1456.
Kobayashi, K., Baba, S., Obayashi. T., Sato, M., Toyooka, K., Keranen, M., Aro, E.M., Fukaki, H., Ohta, H., Sugimoto, K., Masuda, T.,2012. Regulation of Root Greening by Light and Auxin/Cytokinin Signaling in Arabidopsis. The Plant Cell 24,1081-1095.
Koussevitzky, S.. Nott, A., Mockler, T.C., Hong, F., Sachetto-Martins, G., Surpin, M., Lim, J., Mittler, R., Chory, J.,2007. Signals from chloroplasts converge to regulate nuclear gene expression. Science Signaling 316,715.
Krause, G., Weis, E.,1991. Chlorophyll fluorescence and photosynthesis:the basics. Annual review of plant biology 42.313-349.
Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y., Sakakibara, H., Kyozuka, J.,2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445,652-655.
Leivar, P., Monte, E., Cohn. M.M., Quail, P.H.,2012a. Phytochrome Signaling in Green Arabidopsis Seedlings:Impact Assessment of a Mutually Negative phyB-PIF Feedback Loop. Molecular Plant 5.208-223.
Leivar, P., Monte, E., Oka, Y., Liu, T.. Carle, C., Castillon. A., Huq, E., Quail, P.H.,2008. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Current Biology 18,1815-1823.
Leivar. P., Quail, P.H.,2011. PIFs:pivotal components in a cellular signaling hub. Trends in plant science 16,19-28.
Leivar, P., Tepperman, J.M., Cohn, M.M., Monte, E., Al-Sady, B., Erickson, E., Quail, P.H.,2012b. Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. The Plant Cell Online 24,1398-1419.
Leivar, P., Tepperman, J.M., Monte. E., Calderon, R.H., Liu, T.L., Quail, P.H.,2009. Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. The Plant Cell Online 21,3535-3553.
Letham, D., Palni, L.,1983. The biosynthesis and metabolism of cytokinins. Annual review of plant physiology 34,163-197.
Li. C., Bangerth, F.,1992. The possible role of cytokinins, ethylene and indoleacetic acid in apical dominance. Progress in plant growth regulation. Springer, pp.431-436.
Lila, M.A., 2004. Anthocyanins and human health:an in vitro investigative approach. Journal of Biomedicine and biotechnology 2004,306-313.
Lin. C., Ahmad. M., Cashmore, A.R.,1996. Arabidopsis cryptochrome I is a soluble protein mediating blue light-dependent regulation of plant growth and development. The Plant Journal 10, 893-902.
Lin, C., Shalitin, D.,2003. Cryptochrome structure and signal transduction. Annual review of plant biology 54,469-496.
Lin, C., Yang, H., Guo, H., Mockler, T., Chen, J.. Cashmore, A.R.,1998. Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2, Proceedings of the National Academy of Sciences 95.2686-2690.
Lo Piero. A.R., Puglisi. I., Rapisarda, P., Petrone. G.,2005. Anthocyanins accumulation and related gene expression in red orange fruit induced by low temperature storage. Journal of agricultural and food chemistry 53.9083-9088.
Lorrain, S., Trevisan. M.. Pradervand. S.. Fankhauser, C.,2009. Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. The Plant Journal 60, 449-461.
Mas. P.. Devlin, P.F.. Panda, S., Kay. S.A..2000. Functional interaction of phytochrome B and cryptochrome 2. Nature 408,207-211.
Maier. A.. Schrader, A., Kokkelink. L.. Falke. C., Welter, B., Iniesto, E., Rubio, V., Uhrig, J.F., Hulskamp. M., Hoecker. U.,2013. Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcriptions factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. The Plant Journal.
Martinez-Garcia, J., Huq, E., Quail, P.,2000. Direct targeting of light signals to a promoter element-bound transcription factor. Science (New York, NY) 288,859.
Mason. M.G., Mathews, D.E., Argyros. D.A.. Maxwell, B.B., Kieber, J.J., Alonso, J.M., Ecker, J.R., Schaller, G.E.,2005. Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. The Plant Cell Online 17,3007-3018.
Mathews, S., Sharrock, R.,1997. Phytochrome gene diversity. Plant, Cell & Environment 20,666-671.
McDowell. J.M., Dangl, J.L.,2000. Signal transduction in the plant immune response. Trends in biochemical sciences 25,79-82.
Medzihradszky, M., Bindics, J., Adam, E., Viczian, A., Klement, E., Lorrain, S., Gyula, P., Merai, Z., Fankhauser, C. Medzihradszky, K.F.,2013. Phosphorylation of Phytochrome B Inhibits Light-Induced Signaling via Accelerated Dark Reversion in Arabidopsis. The Plant Cell Online.
Millar, A.J., McGrath. R.B., Chua. N.H.,1994. Phytochrome phototransduction pathways. Annu Rev Genet 28,325-349.
Miller, C.O., Skoog, F., Okumura, F.. Von Saltza, M., Strong, F.,1956. Isolation, Structure and Synthesis of Kinetin, a Substance Promoting Cell Division 1,2. Journal of the American Chemical Society 78,1375-1380.
Miller, C.O., Skoog, F.. Von Saltza, M.H., Strong, F.,1955. Kinetin, a cell division factor from deoxyribonucleic acidl. Journal of the American Chemical Society 77,1392-1392.
Mittler, R., Vanderauwera. S., Gollery, M., Van Breusegem, F.,2004. Reactive oxygen gene network of plants. Trends in plant science 9,490-498.
Miwa, H., Kinoshita, A.. Fukuda, H., Sawa, S.,2009. Plant meristems:CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. Journal of plant research 122.31-39.
Mochizuki. N., Tanaka, R., Grimm, B., Masuda, T.. Moulin, M., Smith, A.G., Tanaka. A., Terry, M.J., 2010. The cell biology of tetrapyrroles:a life and death struggle. Trends in plant science 15. 488-498.
Mok, D.W.S., Mok, M.C.,2001. Cytokinin metabolism and action. Annual review of plant biology 52, 89-118.
Monte. E.. Tepperman, J.M., Al-Sady, B., Kaczorowski, K.A., Alonso, J.M., Ecker, J.R.. Li, X.. Zhang, Y., Quail. P.H.,2004. The phytochrome-interacting transcription factor. PIF3. acts early, selectively, and positively in light-induced chloroplast development. Proceedings of the National Academy of Sciences of the United States of America 101.16091-16098.
Nagatani. A., Reed, J.W., Chory, J.,1993. Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiology 102. 269-277.
Nakamura, Y., Kato, T., Yamashino, T., Murakami. M., Mizuno. T., 2007. Characterization of a set of phytochrome-interacting factor-like bHLH proteins in Oryza sativa. Bioscience. biotechnology. and biochemistry 71, 1183-1191.
Neff, M.M., Fankhauser, C, Chory, J., 2000. Light: an indicator of time and place. Genes & Development 14,257-271.
Nesi, N., Jond, C, Debeaujon, I., Caboche. M., Lepiniec, L., 2001. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. The Plant Cell Online 13, 2099-2114.
Nguyen, H.N., Kim, J.H., Hyun, W.Y., Nguyen, N.T., Hong, S.-W., Lee, H., 2013. TTG1-mediated flavonols biosynthesis alleviates root growth inhibition in response to ABA. Plant Cell Reports, 1-12.
Ni, M., Tepperman, J.M., Quail, P.H., 1998. PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95, 657-667.
Ni. M., Tepperman, J.M., Quail. P.H., 1999. Binding of phytochrome B to its nuclear signalling partner P1F3 is reversibly induced by light. Nature 400, 781-784.
NIE, Q., WU, C., LI, J., 2002. Comparison and analysis of stability of several natural anthocynin pigments [J]. Journal of Heilongjiang Commercial College (Natural Sciences Edition) 5,024.
Nishimura, C, Ohashi, Y., Sato, S., Kato, T., Tabata. S., Ueguchi, C, 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. The Plant Cell Online 16, 1365-1377.
Oh, E., Kim, J., Park, E., Kim, J.-I., Kang, C Choi, G., 2004. PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. The Plant Cell Online 16, 3045-3058.
Oh, E., Yamaguchi. S., Kamiya, Y., Bae, G., Chung, W.I., Choi, G., 2006. Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. The Plant Journal 47, 124-139.
Oikawa, K., Kasahara, M., Kiyosue, T., Kagawa, T., Suetsugu. N., Takahashi, F., Kanegae, T., Niwa, Y., Kadota, A., Wada, M., 2003. Chloroplast unusual positioningl is essential for proper chloroplast positioning.. The Plant Cell Online 15, 2805-2815.
Okamoto, H., Matsui, M., Deng, X.W., 2001. Overexpression of the Heterotrimeric G-Protein {{alpha}}-Subunil Enhances Phytochrome-Mediated Inhibition of Hypocotyl Elongation in Arabidopsis. Science Signalling 13, 1639.
Olsen, K.M., Lea, U.S., Slimestad. R., Verheul. M., Lillo, C., 2008. Differential expression of four Arabidopsis PAL genes: PAL1 and PAL2 have functional specialization in abiotic environmental-triggered flavonoid synthesis. Journal of plant physiology 165. 1491-1499.
Olson, E.J., Tabor, J.J., 2012. Post-translational tools expand the scope of synthetic biology. Current Opinion in Chemical Biology.
Oster. U., Tanaka, R., Tanaka, A., Rudiger. W., 2000. Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. The Plant Journal 21. 305-310.
Ozeki, Y., Komamine, A., 1986. Effects of growth regulators on the induction of anthocyanin synthesis in carrot suspension cultures. Plant and Cell Physiology 27, 1361-1368.
Park, E., Kim, J., Lee. Y., Shin, J., Oh, E., Chung, W.-J., Liu, J.R., Choi, G., 2004. Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling. Plant and Cell Physiology 45. 968-975.
Pattanayak, G.K., Biswal, A.K., Reddy, V.S., Tripathy, B.C., 2005. Light-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants. Biochemical and biophysical research communications 326, 466-471.
Pourcel, L., Bohorquez-Restrepo, A., Irani, N.G., Grotewold, E., 2012. Anthocyanin biosynthesis, regulation, and transport: new insights from model species. Recent advances in polyphenol research 3, 143-161.
Qineng, L., 2007. Preliminary Study on Categories, Contents and Stability of Anthocyanins from Potatoes. Journal of Anhui Agricultural Sciences 35, 4811.
Quail, P.H., 1991. Phytochrome: a light-activated molecular switch that regulates plant gene expression. Annu Rev Genet 25, 389-409.
Quail, P.H., 2000. Phytochrome-interacting factors. Semin Cell Dev Biol 11, 457-466.
Quail, P.H., 2002. Phytochrome Photosensory Signalling Networks. Nature Reviews Molecular Cell Biology 3, 85-93.
Rudiger, W., 2002. Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynthesis Research 74, 187-193.
Ramsay, N.A., Glover, B.J., 2005. MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in plant science 10, 63-70.
Ravaglia, D., Espley. R.V., Henry-Kirk, R.A., Andreotti, C, Ziosi, V., Hellens, R.P., Costa, G., Allan, A.C., 2013. Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC plant biology 13, 68.
Reddy, A.M., Reddy. V.S., Scheffler, B.E., Wienand, U., Reddy, A.R., 2007. Novel transgenic rice overexpressing anthocyanidin synthase accumulates a mixture of flavonoids leading to an increased antioxidant potential. Metabolic engineering 9, 95-111.
Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M., Chory, J., 1993. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. The Plant Cell Online 5, 147-157.
Reinbothe, S., Reinbothe. C., Lebedev, N., Apel,. K., 1996. PORA and PORB. two light-dependent protochlorophyllide-reducing enzymes of angiosperm chlorophyll biosynthesis. The Plant Cell 8. 763.
Richter, R., Behringer, C., Muller, I.K., Schwechheimer, C, 2010. The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELL A proteins and PHYTOCHROME-INTERACTING FACTORS. Genes & Development 24, 2093-2104.
Rosati. C, Simoneau, P., Treutter. D., Poupard, P., Cadot, Y., Cadic, A., Duron, M., 2003. Engineering of flower color in forsythia by expression of two independently-transformed dihydroflavonol 4-reductase and anthocyanidin synthase genes of flavonoid pathway. Molecular breeding 12,. 197-208.
Roy. A., Sahoo. D., Tripathy, B.C., 2013. Involvement of phytochrome A in suppression of photomorphogenesis in rice seedling grown in red light. Plant. Cell & Environment.
Sakakibara. H., 2006. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57, 431-449.
Sakamoto. K., Nagatani. A., 1996. Nuclear localization activity of phytochrome B. The Plant Journal 10,859-868.
Sentandreu. M., Martin. G., Gonzalez-Schain, N., Leivar, P., Soy. J., Tepperman, J.M., Quail, P.H., Monle. E.,2011, Functional profiling identifies genes involved in organ-specific branches of the P1F3 regulatory network in Arabidopsis. The Plant Cell Online 23,3974-3991.
Shen, H.. Zhu. L.. Castillon, A., Majee, M., Downie. B., Huq. E.,2008. Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. The Plant Cell Online 20,1586-1602.
Shi. M.-Z., Xie, D.-Y.,2010. Features of anthocyanin biosynthesis in papl-D and wild-type Arabidopsis thaliana plants grown in different light intensity and culture media conditions. Planta 231,1385-1400.
Shin, J., Kim, K., Kang, H., Zulfugarov, I.S., Bae, G., Lee, C.H., Lee, D., Choi, G.,2009. Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proceedings of the National Academy of Sciences 106, 7660-7665.
Shin, J., Park. E.. Choi. G.,2007. PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. The Plant Journal 49,981-994.
Short, T.W., Briggs, W.R.,1994. The transduction of blue light signals in higher plants. Annual review of plant biology 45,143-171.
Siegelman, H., Hendricks, S.,1958. Photocontrol of Anthocyanin Synthesis in Apple Skin. Plant Physiology 33,185.
Skoog, F., Armstrong, D.J.,1970. Cytokinins. Annual review of plant physiology 21,359-384.
Skoog, F., Miller, C.,1957. Chemical regularion of growth and organ formation in plant Tissue cultured, In vitro. Symp. Soc. Exp. Biol., v.11, p.118-131.
Smith, H.,2000. Phytochromes and light signal perception by plants-an emerging synthesis. Nature 407, 585-591.
Springob, K., Nakajima, J.-i., Yamazaki, M., Saito, K.,2003. Recent advances in the biosynthesis and accumulation of anthocyanins. Nat. Prod. Rep.20,288-303.
Stephenson, P.G., Fankhauser. C., Terry, M.J.,2009. PIF3 is a repressor of chloroplast development. Proceedings of the National Academy of Sciences 106,7654-7659.
Sweere, U., Eichenberg, K., Lohrmann, J., Mira-Rodado, V., Baurle,J., Kudla, J., Nagy, F., Schafer, E., Harter, K.,2001. Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science Signalling 294,1108.
Turlerinde, F.C.K.B.A., Klorofil-A. B., Saptanmasi, I.S., Spectrophotometric Determination of Chlorophyll-A. B and Total Carotenoid Contents of Some Algae Species Using Different Solvents.
Takei, K., Sakakibara, H., Sugiyama, T.,2001. Identification of Genes Encoding Adenylate Isopentenyltransferase. a Cytokinin Biosynthesis Enzyme, inArabidopsis thaliana. Journal of Biological Chemistry 276,26405-26410.
Takei, K.. Yamaya. T., Sakakibara, H.,2004. Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. Journal of Biological Chemistry 279,41866-41872.
Tanaka. Y., Sano, T., Tamaoki, M., NAkajima, N., Kondo, N., Hasezawa. S..2006. Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing elhylene production in Arabidopsis. Journal of Experimental Botany 57. 2259-2266.
Tang, W., Wang, W., Chen, D., Ji. Q., Jing, Y., Wang,. H., Lin. R., 2012. Transposase-Derived Proteins FHY3/FAR1 Interact with PHYTOCHROME-INTERACTING FACTOR 1 to Regulate Chlorophyll Biosynthesis by Modulating HEMB1 during Deetiolation in Arabidopsis. The Plant Cell 24, 1984-2000.
Teng, S., Keurentjes, J., Bentsink. L., Koornneef, M., Smeekens. S., 2005. Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiology 139, 1840-1852.
Tepperman, J.M., Hwang, Y.S., Quail, P.H., 2006. phyA dominates in transduction of red - light signals to rapidly responding genes at the initiation of Arabidopsis seedling de - etiolation. The Plant Journal 48, 728-742.
To, J.P., Haberer, G., Ferreira, F.J., Deruere, J., Mason, M.G., Schaller, G.E., Alonso, J.M., Ecker, J.R., Kieber, J.J., 2004. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. The Plant Cell Online 16, 658-671.
Tocttcher. J.E., Gong. D., Lim, W.A., Weiner, O.D., 2011. Light-based feedback for controlling intracellular signaling dynamics. Nature methods 8, 837-839.
Ullah, H., Chen, J.G., Young, J.C., Im, K.H., Sussman, M.R., Jones. A.M., 2001. Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science Signalling 292, 2066.
Vanstraelen, M., Benkova, E., 2012. Hormonal interactions in the regulation of plant development. Annual review of cell and developmental biology 28. 463-487.
von Gromoff, E.D., Alawady, A., Meinecke. L., Grimm, B., Beck, C.F., 2008. Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. The Plant Cell Online 20, 552-567.
Wang. Q., Fristedt, R., Yu, X., Chen. Z., Liu, H., Lee. Y., Guo, H., Merchant. S.S., Lin, C., 2012. The γ-carbonic anhydrase subcomplex of mitochondrial complex I is essential for development and important for photomorphogenesis of Arabidopsis. Plant Physiology 160, 1373-1383.
Werner. T., Motyka, V., Laucou. V., Smets, R., Van Onckelen, H., Schmulling, T., 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. The Plant Cell Online 15, 2532-2550.
Whitelam, G.C., Johnson. E., Peng, J., Carol, P., Anderson, M.L., Cowl, J.S., Harberd, N.P., 1993. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. The Plant Cell Online 5, 757-768.
Xie. D.-Y., Jackson. L.A., Cooper. J.D., Ferreira, D., Paiva. N.L., 2004. Molecular and biochemical analysis of two cDNA clones encoding dihydroflavonol-4-reductase from Medicago truncatula. Plant Physiology 134, 979-994.
Yamaguchi, R., Nakamura, M., Mochizuki, N., Kay, S.A., Nagatani. A., 1999. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. The Journal of cell biology 145, 437-445.
Yanai, O., Shani. E., Dolezal. K., Tarkowski. P., Sablowski. R., Sandberg. G., Samach. A., Ori, N., 2005. Arabidopsis KNOXI Proteins Activate Cytokinin Biosynthesis, Current Biology 15, 1566-1571.
Yang, T., Poovaiah, B., 2003. Calcium/calmodulin-mediated signal network in plants. Trends in plant science 8, 505.
Zhang, Y., Mayba, O., PfeilTer, A., Shi, H., Teppcrman, J.M., Speed, T.P., Quail, P.H., 2013. A Quartet of P1F bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in Arabidopsis. PLOS Genetics 9, e1003244.
Zhao, Z., Andersen, S.U., Ljung, K.., Dolezal, K., Miotk, A., Schultheiss, S.J., Lohmann, J.U., 2010. Hormonal control of the shoot stem-cell niche. Nature 465. 1089-1092.
Zheng, X., Wu, S., Zhai, H., Zhou, P., Song, M., Su, L., Xi. Y., Li. Z., Cai, Y., Meng, F., 2013. Arabidopsis Phytochrome B Promotes SPA1 Nuclear Accumulation to Repress Photomorphogenesis under Far-Red Light. The Plant Cell Online 25, 115-133.
Zhou, Y., Guo. D., Li. J., Cheng, J., Zhou, H., Gu, C., Gardiner, S., Han, Y.-P., 2013. Coordinated regulation of anthocyanin biosynthesis through photorespiration and temperature in peach (Prunus persica f. atropurpurea). Tree Genetics & Genomes 9, 265-278.
Zhu. Y., Tepperman, J.M., Fairchild, CD., Quail, P.H., 2000. Phytochrome B binds with greater apparent affinity than phytochrome A to the basic helix-loop—helix factor PIF3 in a reaction requiring the PAS domain of P1F3. Proceedings of the National Academy of Sciences 97, 13419-13424.