Abstract
Chalcone isomerase-like (CHIL) belongs to the type IV CHI proteins whose roles in cell remain largely unclear. In the present study, we characterized an AcCHIL gene encoding Actinidia chrysantha CHIL protein. The very similar gene structure organization and high sequence identity of AcCHIL with the only two functionally reported CHIL genes (Japanese morning glory InCHIL and Arabidopsis AtCHIL) suggest a similar role of AcCHIL with AtCHIL and InCHIL in promoting flavonoid production and flower pigmentation. The spatial expression analysis shows that AcCHIL gene is expressed predominantly in leaves and stems of A. chrysantha. Consistent with the typical predicted low-temperature-responsive element, abscisic acid (ABA)-responsive element and heat stress-responsive element in the promoter sequence of AcCHIL, the expression of AcCHIL gene in leaves and stems of A. chrysantha, and in petals of A. eriantha are significantly up-regulated by low-temperature and exogenous ABA, but down-regulated by heat stress, though the mRNA levels of AcCHIL in petals of A. chrysantha are always weak and not affected by those stresses. Pink-red petals of A. eriantha instead of golden-yellow petals of A. chrysantha accumulated substantial anthocyanin in response to low temperature and exogenous ABA. Heat stress decreased the anthocyanin accumulation in A. eriantha petals. Interestingly, the content of a yellow colored chalcone, chalcone 2’-glucoside in golden-yellow petals of A. chrysantha is significantly higher than that in pink-red petals of A. eriantha under both the stressed and control conditions. A close correlation between the low levels of AcCHIL mRNA and high levels of accumulated yellow colored chalcone 2’-glucoside in A. chrysantha petals gives an explanation for the formation of distinctive golden-yellow petals in A. chrysantha.
Acknowledgements
This study was jointly supported by the grants from Guangdong Natural Science Foundation (approved Nos 2016A030313370 and 9251022501000001) and Key Lab for Modernization of Characteristic Agriculture in Guangdong Province [(2015)118].
References
Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool.J. Mol. Biol. 215: 403–410.10.1016/S0022-2836(05)80360-2Search in Google Scholar
Arnold K., Bordoli L., Kopp J. & Schwede T. 2006. The SWISSMODEL workspace: A web-based environment for protein structure homology modeling. Bioinformatics 22: 195–201.10.1093/bioinformatics/bti770Search in Google Scholar PubMed
Appelhagen I., Thiedig K., Nordholt N., Schmidt N., Huep G., Sagasser M. & Weisshaar B. 2014. Update on transparent testa mutants from Arabidopsis thaliana: characterisation of new alleles from an isogenic collection. Planta 240: 955–970.10.1007/s00425-014-2088-0Search in Google Scholar PubMed
Crowhurst R.N., Gleave A.P., MacRae E.A., Ampomah-Dwamena C., Atkinson R.G., Beuning L.L., Bulley S.M., Chagne D., Marsh K.B., Matich A.J., and other 35 authors. 2008. Analysis of expressed sequence tags from Actinidia: applications of a cross species EST data base for gene discovery in the areas of flavor, health, color and ripening. BMC Genomics 9(1):351.10.1186/1471-2164-9-351Search in Google Scholar PubMed PubMed Central
Dastmalchi M. & Dhaubhadel S. 2015. Soybean chalcone isomerase: evolution of the fold, and the differential expression and localization of the gene family. Planta 241(2): 507-523.10.1007/s00425-014-2200-5Search in Google Scholar PubMed
Davies K.M., Bloor S.J., Spiller G.B. & Deroles S.C. 1998. Production of yellow color in flowers: redirection of flavonoid biosynthesis in Petunia. Plant J. 13: 259–266.10.1046/j.1365-313X.1998.00029.xSearch in Google Scholar
Ferreyra F.M.L., Rius S.P. & Casati P. 2012. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front. Plant Sci. 3: 222.Search in Google Scholar
Fraser L.G., Seal A.G., Montefiori M., McGhie T.K., Tsang G.K., Datson P.M., Hilario E., Marsh H.E., Dunn J.K., Hellens R.P., Davies K.M., McNeilage M.A., De Silva H.N. & Allan A.C. 2013. An R2R3 MYB transcription factor determines red petal colour in an Actinidia (kiwifruit) hybrid population. BMC Genomics 14: 28.10.1186/1471-2164-14-28Search in Google Scholar PubMed PubMed Central
Gong H.J., Li J.W., Jiang Q.S., Zhang J.C. & Ye K.Y. 2012. Analysis on the characteristics of the dominant community of rare and endangered plant Actinidia chrysantha. J. Zhejiang A & F University 29(2): 301–306.Search in Google Scholar
Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57: 761–780.10.1146/annurev.arplant.57.032905.105248Search in Google Scholar PubMed
Hartmann U., Sagasser M., Mehrtens F., Stracke R. & Weisshaar B. 2005. Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol. Biol. 57: 155–171.10.1007/s11103-004-6910-0Search in Google Scholar PubMed
Hassan S. & Mathesius U. 2012. The role of flavonoids in root–rhizospheresignalling: opportunities and challenges for improving plant–microbe interactions. J. Exp. Bot. 63: 3429–3444.10.1093/jxb/err430Search in Google Scholar PubMed
Higo K., Ugawa Y., Iwamoto M. & Korenaga T.1999. Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res. 27: 297–300.10.1093/nar/26.1.358Search in Google Scholar PubMed PubMed Central
Huang, H.W. & Ferguson A.R. 2007. Genetic resources of kiwifruit: domestication and breeding. Horticul. Rev. 33: 1-121.10.1002/9780470168011.ch1Search in Google Scholar
Jez J.M., Bowman M.E., Dixon R.A. & Noel J.P. 2000. Evolution of the chalcone isomerase fold from fatty-acid binding to stereospecific catalysis; nature, structure and mechanism of the evolutionarily unique plant enzyme chalcone isomerase. Nat. Struct. Mol. Biol. 7: 786–791.10.1038/79025Search in Google Scholar PubMed
Jiang W., Yin Q., Wu R., Zheng G., Liu J., Dixon R.A. & Pang Y. 2015. Role of a chalcone isomerase-like protein in flavonoid biosynthesis in Arabidopsis thaliana. J. Exp. Bot. 66: 7165–7179.10.1093/jxb/erv413Search in Google Scholar PubMed PubMed Central
Lai B., Li X.J., Hu B., Qin Y.H., Huang X.M., Wang H.C. & Hu G.B. 2014. LcMYB1 is a key determinant of differential anthocyanin accumulation among genotypes, tissues, developmental phases and ABA and light stimuli in Litchi chinensis. PLoS ONE 9(1):e86293. 10.1371/journal.pone.0086293.Search in Google Scholar PubMed PubMed Central
Lescot M., Ddhais P., Thijs G., Marchal K., Moreau Y., van de Peer Y., Rouzd P. & Rombauts S. 2002. PlantCARE: A PlantCARE: A database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30: 325–327.10.1093/nar/30.1.325Search in Google Scholar PubMed PubMed Central
Lin-Wang K., Micheletti D., Palmer J., Volz R., Lozano L., Espley R., Hellens R.P., Chagne D., Rowan D.D., Troggio M., Iglesias I. & Allan A.C. 2011. High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant Cell Environ. 34: 1176–1190.10.1111/j.1365-3040.2011.02316.xSearch in Google Scholar PubMed
Liu S., Lv Y., Wan X.R., Li L.M. Hu B. & Li L. 2014. Cloning and expression analysis of cDNAs encoding ABA 8’-hydroxylase in peanut plants in response to osmotic stress. PLoS ONE 9(5), e97025. 10.1371/journal.pone.0097025.Search in Google Scholar PubMed PubMed Central
Morita Y., Takagi K., Fukuchi-Mizutani M., Ishiguro K., Tanaka Y., Nitasaka E., Nakayama M., Saito N., Kagami T., Hoshino A. & Iida S. 2014. A chalcone isomerase-like protein enhances flavonoid production and flower pigmentation. Plant J. 78: 294–304.10.1111/tpj.12469Search in Google Scholar PubMed
Muir S., Collins G., Robinson S., Hughes S., Bovy A., DeVos C., vanTunen A. & Verhoeyen M. 2001. Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat. Biotechnol. 19: 470–474.10.1038/88150Search in Google Scholar PubMed
Muller P.Y., Janovjak H., Miserez A.R. & Dobbie Z. 2002. Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32: 1372–1379.Search in Google Scholar
Ngaki M.N., Louie G.V., Philippe R.N., Manning G., Pojer F., Bowman M.E., Li L., Larsen E., Wurtele E.S. & Noel J.P. 2012. Evolution of the chalcone isomerase fold from fattyacid binding to stereospecific catalysis. Nature 485(7399): 530–533.10.1038/nature11009Search in Google Scholar PubMed PubMed Central
Przysiecka Ł., Ksiazkiewicz M., Wolko B. & Naganowska B. 2015. Structure, expression profile and phylogenetic inference of chalcone isomerase-like genes from the narrow-leafed lupin (Lupinus angustifolius L.) genome. Front. Plant Sci. 6: 268. 10.3389/fpls.2015.00268.Search in Google Scholar PubMed PubMed Central
Ralston L., Subramanian S., Matsuno M. & Yu O. 2005. Partial reconstruction of flavonoid and isoflavonoid biosynthesis in yeast using soybean type I and type II chalcone isomerases. Plant Physiol. 137: 1375–1388.10.1104/pp.104.054502Search in Google Scholar PubMed PubMed Central
Saito N., Tatsuzawa F., Hoshino A., Abe Y., Ichimura M., Yokoi M., Toki K., Morita Y., Iida S. & Honda T. 2011. Anthocyanin pigmentation controlled by speckled and c–1 mutations of Japanese morning glory. J. Jpn. Soc. Hort. Sci. 80: 452–460.10.2503/jjshs1.80.452Search in Google Scholar
Saito R., Fukuta N., Ohmiya A., Itoh Y., Ozeki Y., Kuchitsu K. & Nakayama M. 2006. Regulation of anthocyanin biosynthesis involved in formation of marginal picotee petals in Petunia. Plant Sci. 170: 828–834.10.1016/j.plantsci.2005.12.003Search in Google Scholar
Schwede T., Kopp J., Guex N. & Peitsch M.C. 2003. SWISSMODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31: 3381–3385.10.1093/nar/gkg520Search in Google Scholar PubMed PubMed Central
Shen X., Zhao K., Liu L., Zhang K., Yuan H., Liao X., Wang Q., Guo X., Li F. & Li T. 2014. A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red colored sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol. 55: 862–880.10.1093/pcp/pcu013Search in Google Scholar PubMed
Shimada N., Aoki T., Sato S., Nakamura Y., Tabata S. & Ayabe S. 2003. A cluster of genes encodes the two types of chalcone isomerase involved in the biosynthesis of general flavonoids and legume-specific 5-deoxy (iso) flavonoids in Lotus japonica. Plant Physiol. 131: 941-951.10.1104/pp.004820Search in Google Scholar PubMed PubMed Central
Tamura K., Dudley J., Nei M. & Kumar S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596–1599.10.1093/molbev/msm092Search in Google Scholar PubMed
Tanaka Y., Sasaki N. & Ohmiya A. 2008. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 54: 733–749.10.1111/j.1365-313X.2008.03447.xSearch in Google Scholar PubMed
Varkonyi-Gasic E., Moss S.M., Voogd C., Wu R., Lough R.H., Wang Y.Y. & Hellens R.P. 2011. Identification and characterization of flowering genes in kiwifruit: sequence conservation and role in kiwifruit flower development. BMC Plant Biol. 11: 72—86.10.1186/1471-2229-11-72Search in Google Scholar PubMed PubMed Central
Wan X. & Li L. 2005. Molecular cloning and characterization of a dehydration-inducible cDNA encoding a putative 9 cisepoxycarotenoid dioxygenase in Arachis hypogaea L. DNA Seq. 16: 217–223.10.1080/10425170500129785Search in Google Scholar PubMed
Wan X. & Li L. 2006. Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9 cis-epoxycarotenoid dioxygenase gene. Biochem. Biophys. Res. Commun. 347: 1030–1038.10.1016/j.bbrc.2006.07.026Search in Google Scholar PubMed
Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126: 485–493.10.1104/pp.126.2.485Search in Google Scholar PubMed PubMed Central
Xie X.B., Li S., Zhang R.F., Zhao J., Chen Y.C., Zhao Q., Yao Y.X., You C.X., Zhang X.S. & Hao Y.J. 2012. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ. 35: 1884–1897.10.1111/j.1365-3040.2012.02523.xSearch in Google Scholar PubMed
Yonekura-Sakakibara K., Fukushima A., Nakabayashi R., Hanada K., Matsuda F., Sugawara S., Inoue E., Kuromori T., Ito T., Shinozaki K. Wangwattana B., Yamazaki M. & Saito K. 2012. Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana. Plant J. 69: 154–167.10.1111/j.1365-313X.2011.04779.xSearch in Google Scholar PubMed PubMed Central
Yonekura-Sakakibara K., Tohge T., Matsuda F., Nakabayashi R., Takayama H., Niida R., Watanabe-Takahashi A., Inoue E. & Saito K. 2008. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding genemetabolite correlations in Arabidopsis. Plant Cell 20: 2160–2176.10.1105/tpc.108.058040Search in Google Scholar PubMed PubMed Central
Zeng M.H., Liu S.H., Yang M.X., Zhang Y.J., Liang J.Y., Wan X.R. & Liang H. 2013. Characterization of a gene encoding clathrin heavy chain in maize up-regulated by salicylic acid, abscisic acid and high boron supply. Int. J. Mol. Sci. 14: 15179-15198.10.3390/ijms140715179Search in Google Scholar PubMed PubMed Central
Zhang H., Liu J., Lu, H. & Gao S. 2009. Enhanced flavonoid production in hairy root cultures of Glycyrrhiza uralensis Fisch by combining the over-expression of chalcone isomerase gene with the elicitation treatment. Plant Cell Rep. 28: 1205–1213.10.1007/s00299-009-0721-3Search in Google Scholar PubMed
© 2017 Institute of botany, Slovak Academy of Sciences
Articles in the same Issue
- Botany
- Comparative morphoanatomical analysis of the leaves and stems of Daphne (Thymelaeaceae) species
- Botany
- Effect of the Gabčíkovo Waterworks (Slovakia) on riparian floodplain forest ecosystems in the Danube inland delta: vegetation dynamics and trends
- Botany
- Effects of different light qualities on seedling growth and chlorophyll fluorescence parameters of Dendrobium officinale
- Botany
- Identification and expression analyses of two lotus (Nelumbo nucifera) dehydrin genes in response to adverse temperatures, ABA and IAA treatments
- Botany
- Characterization and expression analysis of a chalcone isomerase-like gene in relation to petal color of Actinidia chrysantha
- Cellular and Molecular Biology
- Citrus flavonoids collectively dominate the α-amylase and α-glucosidase inhibitions
- Zoology
- Distribution, diversity and some ecological characteristics of ostracods (Crustacea: Ostracoda) in Gökçeada (Imbros) Island (Northern Aegean Sea, Turkey)
- Zoology
- Native crab and crayfish co-occurrence: First evidence in Europe
- Zoology
- DNA barcoding and first records of two rare Adicella species (Trichoptera: Leptoceridae) in Croatia
- Zoology
- Occurrence of Tomicobia seitneri (Hymenoptera: Pteromalidae) and Ropalophorus clavicornis (Hymenoptera: Braconidae) in Ips typographus adults (Coleoptera: Curculionidae: Scolytinae) from Austria, Poland and France
- Zoology
- Cockroach forewing area and venation variabilities relate
- Zoology
- First data on the population of the European pond turtle Emys orbicularis at Lake Tonga, El Kala National Park, Algeria
Articles in the same Issue
- Botany
- Comparative morphoanatomical analysis of the leaves and stems of Daphne (Thymelaeaceae) species
- Botany
- Effect of the Gabčíkovo Waterworks (Slovakia) on riparian floodplain forest ecosystems in the Danube inland delta: vegetation dynamics and trends
- Botany
- Effects of different light qualities on seedling growth and chlorophyll fluorescence parameters of Dendrobium officinale
- Botany
- Identification and expression analyses of two lotus (Nelumbo nucifera) dehydrin genes in response to adverse temperatures, ABA and IAA treatments
- Botany
- Characterization and expression analysis of a chalcone isomerase-like gene in relation to petal color of Actinidia chrysantha
- Cellular and Molecular Biology
- Citrus flavonoids collectively dominate the α-amylase and α-glucosidase inhibitions
- Zoology
- Distribution, diversity and some ecological characteristics of ostracods (Crustacea: Ostracoda) in Gökçeada (Imbros) Island (Northern Aegean Sea, Turkey)
- Zoology
- Native crab and crayfish co-occurrence: First evidence in Europe
- Zoology
- DNA barcoding and first records of two rare Adicella species (Trichoptera: Leptoceridae) in Croatia
- Zoology
- Occurrence of Tomicobia seitneri (Hymenoptera: Pteromalidae) and Ropalophorus clavicornis (Hymenoptera: Braconidae) in Ips typographus adults (Coleoptera: Curculionidae: Scolytinae) from Austria, Poland and France
- Zoology
- Cockroach forewing area and venation variabilities relate
- Zoology
- First data on the population of the European pond turtle Emys orbicularis at Lake Tonga, El Kala National Park, Algeria