Photosynthetica 2019, 57(3):866-874 | DOI: 10.32615/ps.2019.078
Proteomic analysis of chloroplasts from chlorophyll-deficient melon mutant
- 1 Horticulture College, Northeast Agricultural University, No. 59 Mucai Street, Heilongjiang Province, 150030 Harbin, China
- 2 Harbin Academy of Agricultural Science, Harbin, China
- 3 Life Science and Technology Institute, Harbin Normal University, Harbin, China
We aimed to understand the molecular-level changes occurring in the photosynthetic metabolic network in mutant chloro-plasts. We performed comparative liquid chromatography-mass spectrometry protein profiling of wild-type (WT) and chlorophyll-deficient melon (Cucumis melo L.) mutants. We identified 390 differentially expressed proteins and 81 shared proteins varied significantly in abundance, of which 76 were upregulated and 5 were downregulated. Differentially expressed proteins were involved in the following biological processes: binding, catalytic, structural, transporter, and antioxidant activities. The mutant had 6.08-fold higher expression of glutamate-1-semialdehyde 2,1-aminomutase (GSAM), an enzyme that synthesizes the chlorophyll precursor, 5-aminolevulinic acid, and a 5.02-fold higher expression of pyridoxal biosynthesis protein, a GSAM coenzyme. An RNA recognition motif-containing protein (RRM) decreased in expression by 5.22-fold. This suggests that GSAM and RRM are particularly relevant to chlorophyll deficiency.
Additional key words: label-free protein quantification; photosynthetic pathways; proteome analysis; qRT-PCR.
Received: May 25, 2018; Accepted: November 28, 2018; Prepublished online: July 12, 2019; Published: July 23, 2019 Show citation
Supplementary files
| Download file | Zhao 1949 supplement.docx File size: 1.12 MB |
References
- Aubry S., Brown N.J., Hibberd J.M.: The role of proteins in C3 plants prior to their recruitment into the C4 pathway. - J. Exp. Bot. 62: 3049-3059, 2011.
Go to original source... - Bansal M., Sharma M., Kanwar P., Goyal A.: Recent advances in proteomics of cereals.- Biotechnol. Genet. Eng. 32: 1-17, 2016.
Go to original source... - Bollivar D.W.: Recent advances in chlorophyll biosynthesis. - Photosynth. Res. 90: 173-194, 2006.
Go to original source... - Brestic M., Zivcak M., Kunderlikova K. et al.: Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. - Photosynth. Res. 125: 151-166, 2015.
Go to original source... - Brunkard J.O., Runkel A.M., Zambryski P.C.: Chloroplasts extend stromules independently and in response to internal redox signals. - P. Natl. Acad. Sci. USA 112: 10044-10049, 2015.
Go to original source... - Caffarri S., Tibiletti T., Jennings R.C., Santabarbara S.: A com-parison between plant photosystem I and photosystem II architecture and functioning. - Curr. Protein Pept. Sc. 15: 296-331, 2014.
Go to original source... - Caplan J.L., Kumar A.S., Park E. et al.: Chloroplast stromules function during innate immunity. - Dev. Cell. 34: 45-57, 2015.
Go to original source... - Carvalho R.F., Takaki M., Azevedo R.A.: Plant pigments: the many faces of light perception. - Acta Physiol. Plant. 33: 241-248, 2011.
Go to original source... - Chang T.E., Wegmann B., Wang W.Y.: Purification and charac-terization of glutamyl-tRNA synthetase: An enzyme involved in chlorophyll biosynthesis. - Plant Physiol. 93: 1641-1649, 1990.
Go to original source... - Cline K.: Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. - J. Biol. Chem. 261: 14804-14810, 1986.
Go to original source... - Erb T.J., Zarzycki J.: A short history of RubisCO: the rise and fall (?) of Nature's predominant CO2 fixing enzyme. - Curr. Opin. Biotech. 49:100-107, 2017.
Go to original source... - Espineda C.E., Linford A.S., Devine D., Brusslan J.A.: The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. - P. Natl. Acad. Sci. USA 96: 10507-10511, 1999.
Go to original source... - Fesenko I., Seredina A., Arapidi G. et al.: The Physcomitrella patens chloroplast proteome changes in response to proto-plastation. - Front. Plant Sci. 7: 1661, 2016.
Go to original source... - Fu Y., Duan X., Tang C., Wang X. et al.: TaADF7, an actin-depolymerizing factor, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. - Plant J. 78: 16-30, 2014.
Go to original source... - Gasperini D., Chauvin A., Acosta I.F. et al.: Axial and radial oxylipin transport. - Plant Physiol. 169: 2244-2254, 2015.
Go to original source... - Gontero B., Cárdenas M.L., Ricard J.: A functional five-enzyme complex of chloroplasts involved in the Calvin cycle. - Eur. J. Biochem. 173: 437-443, 1988.
Go to original source... - Greene B.A., Allred D.R., Morishige D.T., Staehelin L.A.: Hierarchical response of light harvesting chlorophyll-proteins in a light-sensitive chlorophyll b-deficient mutant of maize. - Plant. Physiol. 87: 357-364, 1988.
Go to original source... - Gubernator B., Króliczewski J., Kallas T., Szczepaniak A.: Iron-sulfur cluster reconstitution of spinach chloroplast Rieske protein requires a partially prefolded apoprotein. - BBA-Proteins Proteom. 1764: 735-742, 2006.
Go to original source... - Hedtke B., Alawady A., Chen S. et al.: HEMA RNAi silencing reveals a control mechanism of ALA biosynthesis on Mg chelatase and Fe chelatase. - Plant Mol. Biol. 64: 733-742, 2007.
Go to original source... - Henty-Ridilla J.L., Li J., Day B., Staiger C.J.: ACTIN DEPOLY-MERIZING FACTOR4 regulates actin dynamics during innate immune signaling in Arabidopsis. - Plant Cell 26: 340-352, 2014.
Go to original source... - Hricová A., Quesada V., Micol J.L.: The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. - Plant Physiol. 141: 942-956, 2006.
Go to original source... - Jain M., Nijhawan A., Tyagi A.K., Khurana J.P.: Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. - Biochem. Bioph. Res. Co. 345: 646-651, 2006.
Go to original source... - Jakhar S., Mukherjee D.: Chloroplast pigments, proteins, lipid peroxidation and activities of antioxidative enzymes during maturation and senescence of leaves and reproductive organs of Cajanus cajan L. - Physiol. Mol. Biol. Pla. 20: 171-180, 2014.
Go to original source... - Jensen P.E., Leister D.: Chloroplast evolution, structure and functions. - F1000Prime Rep. 6: 40, 2014.
Go to original source... - Kim C., Apel K.: Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. - Photosynth. Res. 116: 455-464, 2013.
Go to original source... - Kmiecik P., Leonardelli M., Teige M.: Novel connections in plant organellar signalling link different stress responses and signalling pathways. - J. Exp. Bot. 67: 3793-3807, 2016.
Go to original source... - Kindgren P., Kremnev D., Blanco N.E. et al.: The plastid redox insensitive 2 mutant of Arabidopsis is impaired in PEP activity and high light-dependent plastid redox signalling to the nucleus. - Plant J. 70: 279-291, 2012.
Go to original source... - Kumar A.M., Söll D.: Antisense HEMA1 RNA expression inhibits heme and chlorophyll biosynthesis in Arabidopsis. - Plant Physiol. 122: 49-56, 2000.
Go to original source... - Li N., Jia J., Xia C. et al.: Characterization and mapping of novel chlorophyll deficient mutant genes in durum wheat. - Breeding Sci. 63: 169-175, 2013.
Go to original source... - Li H.S., Sun Q., Zhao S.J. et al.: [The Experiment Principle and Technique on Plant Physiology and Biochemistry.] Pp. 134. Higher Education Press, Beijing 2000. [In Chinese]
- Liu J., Zhou W., Liu G. et al.: The conserved endoribonuclease YbeY is required for chloroplast ribosomal RNA processing in Arabidopsis. - Plant Physiol. 168: 205-221, 2015.
Go to original source... - Liu X., Yu W., Wang G. et al.: Comparative proteomic and physiological analysis reveals the variation mechanisms of leaf coloration and carbon fixation in a xantha mutant of Ginkgo biloba L. - Int. J. Mol. Sci. 17: 1794, 2016.
Go to original source... - Lundquist P.K., Mantegazza O., Stefanski A. et al.: Surveying the oligomeric state of Arabidopsis thaliana chloroplasts. - Mol. Plant 10: 197-211, 2017.
Go to original source... - Mohayeji M., Capriotti A.L., Cavaliere C. et al.: Heterosis profile of sunflower leaves: a label free proteomics approach. - J. Proteomics 99: 101-110, 2014.
Go to original source... - Moser J., Schubert W.D., Beier V. et al.: V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-depen-dent tetrapyrrole biosynthesis. - EMBO J. 20: 6583-6590, 2001.
Go to original source... - Motohashi R., Rödiger A., Agne B. et al.: Common and specific protein accumulation patterns in different albino/pale-green mutants reveals regulon organization at the proteome level. - Plant Physiol. 160: 2189-2201, 2012.
Go to original source... - Natesan S.K., Sullivan J.A., Gray J.C.: Stromules: a characteristic cell-specific feature of plastid morphology. - J. Exp. Bot. 56: 787-797, 2005.
Go to original source... - Peremarti A., Marè C., Aprile A. et al.: Transcriptomic and proteomic analyses of a pale-green durum wheat mutant shows variations in photosystem components and metabolic deficiencies under drought stress. - BMC Genomics 15: 125, 2014.
Go to original source... - Pospí¹il P., Yamamoto Y.: Damage to photosystem II by lipid peroxidation products. - BBA-Gen. Subjects 1861: 457-466, 2017.
Go to original source... - Rochaix J.D., Ramundo S.: Conditional repression of essential chloroplast genes: Evidence for new plastid signaling pathways. - Biochim. Biophys. Acta 1847: 986-992, 2015.
Go to original source... - Rutschow H., Ytterberg A.J., Friso G. et al.: Quantitative proteomics of a chloroplast SRP54 sorting mutant and its genetic interactions with CLPC1 in Arabidopsis. - Plant Physiol. 148: 156-175, 2008.
Go to original source... - Sandonà D., Croce R., Pagano A. et al.: Higher plants light harvesting proteins. Structure and function as revealed by mu- tation analysis of either protein or chromophore moieties. - BBA-Bioenergetics 1365: 207-214, 1998.
Go to original source... - Satou M., Enoki H., Oikawa A. et al.: Integrated analysis of transcriptome and metabolome of Arabidopsis albino or pale green mutants with disrupted nuclear-encoded chloroplast proteins. - Plant Mol. Biol. 85: 411-428, 2014.
Go to original source... - Sawers R.J.H., Linley P.J., Farmer P.R. et al.: Elongated mesocotyl1, a phytochrome-deficient mutant of maize. - Plant Physiol. 130: 155-163, 2002.
Go to original source... - Shao Q., Yu Z.Y., Li X.G. et al.: [Studies on internal physiological and biochemical changes of xantha mutant in melon leaves.] - China Vegetables 14: 59-65, 2013. [In Chinese]
- Singh R., Jwa N.S.: Understanding the responses of rice to environmental stress using proteomics. - J. Proteome Res. 12: 4652-4669, 2013.
Go to original source... - Stoppel R., Meurer J.: Complex RNA metabolism in the chlo-roplast: an update on the psbB operon. - Planta 237: 441-449, 2013.
Go to original source... - Sun T., Germain A., Giloteaux L. et al.: An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize. - P. Natl. Acad. Sci. USA 110: 1169-1178, 2013.
Go to original source... - Timmis J.N., Ayliffe M.A., Huang C.Y., Martin W.: Endo-symbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. - Nat. Rev. Genet. 5: 123-135, 2004.
Go to original source... - Tomiyama M., Inoue S., Tsuzuki T. et al.: Mg-chelatase I subunit 1 and Mg-protoporphyrin IX methyltransferase affect the sto-matal aperture in Arabidopsis thaliana. - J. Plant Res. 127: 553-563, 2014.
Go to original source... - Tripathy B.C., Mohapatra A., Gupta I.: Impairment of the photosynthetic apparatus by oxidative stress induced by photosensitization reaction of protoporphyrin IX. - BBA-Bioenergetics 1767: 860-868, 2007.
Go to original source... - Tsang E.W., Yang J., Chang Q. et al.: Chlorophyll reduction in the seed of Brassica napus with a glutamate 1-semialdehyde aminotransferase antisense gene. - Plant Mol. Biol. 51: 191-201, 2003.
Go to original source... - van Wijk K.J., Peltier J.B., Giacomelli L.: Isolation of chloroplast proteins from Arabidopsis thaliana for proteome analysis. - Method. Mol. Biol. 355: 43-48, 2007.
Go to original source... - Wang L., Yue C., Cao H. et al.: Biochemical and transcriptome analyses of a novel chlorophyll-deficient chlorina tea plant cultivar. - BMC Plant Biol. 14: 352, 2014.
Go to original source... - Yu J., Zhang J., Zhao Q. et al.: Proteomic analysis reveals the leaf color regulation mechanism in chimera Hosta ʻGold Standardʼ leaves. - Int. J. Mol. Sci. 17: 346, 2016.
Go to original source...




