Biologia plantarum 61:255-265, 2017 | DOI: 10.1007/s10535-016-0662-y

Comprehensive analysis of differently expressed genes and proteins in albino and green plantlets from a wheat anther culture

P. Zhao1, K. Wang1, W. Zhang1, H. Y. Liu1, L. P. Du1, H. R. Hu2, X. G. Ye1,*
1 Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, P.R. China
2 College of Life Sciences, Northwest A&F University, Shanxi, Yangling, P.R. China

The anther culture technique, although it has been widely used in wheat breeding programs, is associated with a high albinism rate that limits its application. The mechanism of albinism has not been studied explicitly at the molecular level. In this study, differently expressed genes (DEGs) and proteins (DEPs) of albino and green seedlings from a wheat anther culture were analyzed and compared using transcriptomic sequencing (RNA-Seq), two-dimensional electrophoresis, and mass spectrometry. A total of 1 892 DEGs (1 115 down-regulated and 777 up-regulated) and 43 DEPs (15 down-regulated and 28 up-regulated) that are primarily involved in photosynthetic pathways and porphyrin and chlorophyll metabolism was identified when the albino group library was used as the control. Most DEGs participated in constructing components of thylakoids and the chloroplast envelope as determined via gene ontology analysis. The expression patterns of 12 selected genes were evaluated using real-time quantitative PCR, and the results were in agreement with the RNA-Seq analysis. Our results may assist the development of new methods to decrease the albino seedling rates in wheat anther cultures.

Keywords: chloroplast; photosynthesis; transcriptomic sequencing; Triticum aestivum
Subjects: DEGs; albino plantlets; anther culture; transcriptome analysis; chloroplast; photosynthesis; RNA-seq; wheat
Species: Triticum aestivum

Received: November 17, 2015; Revised: May 3, 2016; Accepted: May 5, 2016; Published: June 1, 2017Show citation

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Zhao, P., Wang, K., Zhang, W., Liu, H.Y., Du, L.P., Hu, H.R., & Ye, X.G. (2017). Comprehensive analysis of differently expressed genes and proteins in albino and green plantlets from a wheat anther culture. Biologia plantarum61(2), 255-265. doi: 10.1007/s10535-016-0662-y.
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References

  1. Andersen, S.B., Due, I.K., Olesen, A.: The response of anther culture in a genetically wide material of winter wheat (Triticum aestivum L.). - Plant Breed. 99: 181-186, 1987. Go to original source...
  2. Andrade-Souza, V., Costa, M.G., Chen, C.X., Gmitter, F.G., Jr., Costa, M.A.: Physical location of the carotenoid biosynthesis genes Psy and beta-Lcy in Capsicum annuum (Solanaceae) using heterologous probes from Citrus sinensis (Rutaceae). - Genet. mol. Res. 10: 404-409, 2011. Go to original source...
  3. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., Harris, M.A., Hill, D.P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J.C., Richardson, J.E., Ringwald, M., Rubin, G.M., Sherlock, G.: Gene ontology: tool for the unification of biology. The gene ontology consortium. - Nat. Genet. 25: 25-29, 2000. Go to original source...
  4. Chou, K.C., Shen, H.B.: Cell-PLoc: a package of Web servers for predicting subcellular localization of proteins in various organisms. - Nat. Protocols 3: 153-162, 2008. Go to original source...
  5. Cistué, L., Vallés, M.P., Echávarri, B., Sanz, J.M., Castillo, A.: Barley anther culture. - In Maluszynski, M., Kasha, K.J., Forster, B.P. Szarejko, I., (ed.): Doubled Haploid Production in Crop Plants. Pp. 29-34. Springer, Dordrecht 2003.
  6. Daie, J.: Cytosolic fructose-1,6-bisphosphatase: a key enzyme in the sucrose biosynthetic pathway. - Photosynth. Res. 38: 5-14, 1993. Go to original source...
  7. Day, A., Ellis, T.H.: Chloroplast DNA deletions associated with wheat plants regenerated from pollen: possible basis for maternal inheritance of chloroplasts. - Cell 39: 359-368, 1984. Go to original source...
  8. Day, A., Ellis, T.H.N.: Deleted forms of plastid DNA in albino plants from cereal anther culture. - Curr. Genet. 9: 671-678, 1985. Go to original source...
  9. De Buyser, J., Henry, Y., Lonnet, P., Hertzog, R., Hespel, A.: 'Florin': a doubled haploid wheat variety developed by the anther culture method. - Plant Breed. 98: 53-56, 1987. Go to original source...
  10. Dunford, R., Walden, R.: Plastid genome structure and plastidrelated transcript levels in albino barley plants derived from anther culture. - Curr. Genet. 20: 339-347, 1991. Go to original source...
  11. Ekman, D.R., Lorenz, W.W., Przybyla, A.E., Wolfe, N.L., Dean, J.F.: SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. - Plant Physiol. 133: 1397-1406, 2003. Go to original source...
  12. Fujita Y., Takagi H., Hase T.: Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and - independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum. - Plant Cell Physiol. 39: 177-185, 1998. Go to original source...
  13. Geiger, D.R., Servaites, J.C.: Diurnal regulation of photosynthetic carbon metabolism in C3 plants. - Annu. Rev. Plant. Physiol. Plant mol. Biol. 45: 235-256, 1994. Go to original source...
  14. Guha, S., Maheshwari, S.C.: In vitro production of embryos from anthers of Datura. - Nature 204: 497-497, 1964. Go to original source...
  15. Harada, T., Sato, T., Asaka, D., Matsukawa, I.: Large-scale deletions of rice plastid DNA in anther culture. - Theor. appl. Genet. 81: 157-161, 1991. Go to original source...
  16. Hershko, A., Ciechanover, A.: The ubiquitin system. - Annu. Rev. Biochem. 67: 425-479, 1998. Go to original source...
  17. Hou, D.Y., Xu, H., Du, G.Y., Lin, J.T., Duan, M., Guo, A.G.: Proteome analysis of chloroplast proteins in stage albinism line of winter wheat (Triticum aestivum) FA85. - BMB Rep. 42: 450-455, 2009. Go to original source...
  18. Hu, D.F., Yuan, Z.D., Tang, Y.L., Liu, J.P.: [Plant cell engineering: development of a new winter wheat variety Jinghua 1 by anther culture.] - Sci. China (Series B) 3: 283-292, 1986. [In Chin.]
  19. Jansson, S.: A guide to the Lhc genes and their relatives in Arabidopsis. - Trends Plant. Sci. 4: 236-240, 1999. Go to original source...
  20. Just, B.J., Santos, C.A., Fonseca, M.E., Boiteux, L.S., Oloizia, B.B., Simon, P.W.: Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping. - Theor. appl. Genet. 114: 693-704, 2007. Go to original source...
  21. Kokubun, N., Ishida, H., Makino, A., Mae, T.: The degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase into the 44-kDa fragment in the lysates of chloroplasts incubated in darkness. - Plant Cell Physiol. 43: 1390-1395, 2002. Go to original source...
  22. Larsen, E.T., Tuvesson, I.K., Andersen, S.B.: Nuclear genes affecting percentage of green plants in barley (Hordeum vulgare L.) anther culture. - Theor. appl. Genet. 82: 417-420, 1991. Go to original source...
  23. Lee S., Kim J.H., Yoo E.S., Lee C.H., Hirochika H., An G.: Differential regulation of chlorophyll a oxygenase genes in rice. - Plant mol. Biol. 57: 805-818, 2005. Go to original source...
  24. Lee, S.K., Jeon, J.S., Bornke, F., Voll, L., Cho, J.I., Goh, C.H., Jeong, S.W., Park, Y.I., Kim, S.J., Choi, S.B., Miyao, A., Hirochika, H., An, G., Cho, M.H., Bhoo, S.H., Sonnewald, U., Hahn, T.R.: Loss of cytosolic fructose-1,6-bisphosphatase limits photosynthetic sucrose synthesis and causes severe growth retardations in rice (Oryza sativa). - Plant Cell Environ. 31: 1851-1863, 2008.
  25. Lefebvre, S., Lawson, T., Zakhleniuk, O.V., Lloyd, J.C., Raines, C.A., Fryer, M.: Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. - Plant Physiol. 138: 451-460, 2005. Go to original source...
  26. Li, R.Q., Yu, C., Li, Y.R., Lam, T.W., Yiu, S.M., Kristiansen, K., Wang, J.: SOAP2: an improved ultrafast tool for short read alignment. - Bioinformatics 25: 1966-1967, 2009.
  27. Lindgren, L.O., Stalberg, K.G., Hoglund, A.S.: Seed-specific overexpression of an endogenous Arabidopsis phytoene synthase gene results in delayed germination and increased levels of carotenoids, chlorophyll, and abscisic acid. - Plant Physiol. 132: 779-785, 2003. Go to original source...
  28. Liu, J.X., Chiou, C.Y., Shen, C.H., Chen, P.J., Liu, Y.C., Jian, C.D., Shen, X.L., Shen, F.Q., Yeh, K.W.: RNA interference-based gene silencing of phytoene synthase impairs growth, carotenoids, and plastid phenotype in Oncidium hybrid orchid. - SpringerPlus 3: 478, 2014b. Go to original source...
  29. Liu, L., Shao, Z., Zhang, M., Wang, Q.: Regulation of carotenoid metabolism in tomato. - Mol. Plant. 8: 28-39, 2014a. Go to original source...
  30. Lopez-Casado, G., Covey, P.A., Bedinger, P.A., Mueller, L.A., Thannhauser, T.W., Zhang, S., Fei, Z., Giovannoni, J.J., Rose, J.K.C.: Enabling proteomic studies with RNA-Seq: the proteome of tomato pollen as a test case. - Proteomics 12: 761-774, 2012. Go to original source...
  31. Meier, S., Tzfadia, O., Vallabhaneni, R., Gehring, C., Wurtzel, E.T.: A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. - BMC Syst. Biol. 5: 77, 2011. Go to original source...
  32. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, B.: Mapping and quantifying mammalian transcriptomes by RNA-Seq. - Nat. Methods. 5: 621-628, 2008. Go to original source...
  33. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M., Snyder, M.: The transcriptional landscape of the yeast genome defined by RNA sequencing. - Science 320: 1344-1349, 2008. Go to original source...
  34. Nick, S., Meurer, J., Soll, J., Ankele, E.: Nucleus-encoded lightharvesting chlorophyll a/b proteins are imported normally into chlorophyll b-free chloroplasts of Arabidopsis. - Mol. Plant. 6: 860-871, 2013. Go to original source...
  35. Oster, U., Tanaka, R., Tanaka, A., Rudiger, W.: Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. - Plant J. 21: 305-310, 2000. Go to original source...
  36. Ouyang, J.W., Hu, H., Zhang, J.J., Zeng, J.Z.: [Induction and investigation of pollen plants and their offspring in wheat.] - Sci. China (Series A). 16: 72-82, 1973. [In Chin]
  37. Ouyang, J.W., Jia, S.E., Zhang, C., Chen, X., and G., F.: [A new synthetic medium (W14) for wheat anther culture.] - Annu. Rep. Inst. Genet. Acad. sin. 91-92, 1989. [In Chin.]
  38. Paulsen, H., Dockter, C., Volkov, A., Jeschke, G.: Folding and pigment binding of light-harvesting chlorophyll a/b protein (LHCIIb). - In: Rebeiz, C., Benning, C., Bohnert, H., Daniell, H., Hoober, J.K., Lichtenthaler, H., Portis, A., Tripathy, B. (ed.): The Chloroplast. Vol. 16. Pp. 231-244. Springer, Dordrecht 2010. Go to original source...
  39. Peng, Y., Zhang, Y., Lv, J., Zhang, J.H., Li, P., Shi, X.L., Wang, Y.F., Zhang, H.L., He, Z.H., Teng, S.: Characterization and fine mapping of a novel rice albino mutant low temperature albino 1. - J. Genet. Genomics 39: 385-396, 2012. Go to original source...
  40. Plumley, G.F., Schmidt, G.W.: Light-harvesting chlorophyll a/b complexes: interdependent pigment synthesis and protein assembly. - Plant Cell 7: 689-704, 1995. Go to original source...
  41. Portis, A.R., Jr.: Rubisco activase - Rubisco's catalytic chaperone. - Photosynth. Res. 75: 11-27, 2003. Go to original source...
  42. Qin, G., Gu, H., Ma, L., Peng, Y., Deng, X.W., Chen, Z., Qu, L.J.: Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. - Cell Res. 17: 471-482, 2007. Go to original source...
  43. Rampino, P., Spano, G., Pataleo, S., Mita, G., Napier, J.A., Di Fonzo, N., Shewry, P.R., Perrotta, C.: Molecular analysis of a durum wheat 'stay green' mutant: expression pattern of photosynthesis-related genes. - J. Cereal Sci. 43: 160-168, 2006. Go to original source...
  44. Ren, X., Ye, X., Xu, H., Dong, J., Du, L., Zhang X.: [Development of new spring wheat variety Ningchun42 by anther culture.] - Crops 2: 19, 2006. [In Chin.]
  45. Schmittgen, T.D., Livak, K.J.: Analyzing real-time PCR data by the comparative C(T) method. - Nat. Protocols 3: 1101-1108, 2008. Go to original source...
  46. Schmitz-Linneweber, C., Williams-Carrier, R.E., Williams-Voelker, P.M., Kroeger, T.S., Vichas, A., Barkan, A.: A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. - Plant Cell 18: 2650-2663, 2006. Go to original source...
  47. Spreitzer, R.J.: Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. - Arch. Biochem. Biophys. 414: 141-149, 2003. Go to original source...
  48. Tang, M.H., Hai, Y., Da, L.Z., Zhou X.B., Zhao Y.Y.: [The breeding and characteristics of new wheat variety Huapei 5.] - Chin. Agr. Sci. Bull. 25: 98-101, 2009. [In Chin.]
  49. Teramoto, H., Ono, T., Minagawa, J.: Identification of Lhcb gene family encoding the light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii. - Plant Cell. Physiol. 42: 849-856, 2001. Go to original source...
  50. Tucker, W.C., Du, Z.Y., Hein, R., Gromet-Elhanan, Z., Richter, M.L.: Role of the ATP synthase alpha-subunit in conferring sensitivity to tentoxin. - Biochemistry 40: 7542-7548, 2001. Go to original source...
  51. Tuvesson, I.K., Pedersen, S., Andersen, S.B.: Nuclear genes affecting albinism in wheat (Triticum aestivum L.) anther culture. - Theor. appl. Genet. 78: 879-883, 1989. Go to original source...
  52. Wang, K., Wang, S., Zhou, X., Lin, Z., Li, J., Du, L., Tang, Y., Xu, H., Yan, Y., Ye, X.: Development, identification, and genetic analysis of a quantitative dwarfing somatic variation line in wheat. - Crop Sci. 53: 1032-1041, 2013. Go to original source...
  53. Wang, L., Feng, Z., Wang, X., Wang, X., Zhang, X.: DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. - Bioinformatics 26: 136-138, 2010. Go to original source...
  54. Wang, Z., Gerstein, M., Snyder, M.: RNA-Seq: a revolutionary tool for transcriptomics. - Nat. Rev. Genet. 10: 57-63, 2009. Go to original source...
  55. Yaronskaya, E., Ziemann, V., Walter, G., Averina, N., Borner, T., Grimm, B.: Metabolic control of the tetrapyrrole biosynthetic pathway for porphyrin distribution in the barley mutant albostrians. - Plant J. 35: 512-522, 2003. Go to original source...
  56. Yosef, I., Irihimovitch, V., Knopf, J.A., Cohen, I., Orr-Dahan, I., Nahum, E., Keasar, C., Shapira, M.: RNA binding activity of the ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit from Chlamydomonas reinhardtii. - J. biol. Chem. 279, 10148-10156, 2004. Go to original source...
  57. Zhan, G.M., Li, R.J., Hu, Z.Y., Liu, J., Deng, L.B., Lu, S.Y., Hua, W.: Cosuppression of RBCS3B in Arabidopsis leads to severe photoinhibition caused by ROS accumulation. - Plant Cell Rep. 33: 1091-1108, 2014. Go to original source...
  58. Zhang, H., Li, J., Yoo, J.H., Yoo, S.C., Cho, S.H., Koh, H.J.: Rice Chlorine-1 and Chlorina-9 encode ChID and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. - Plant mol. Biol. 62: 325-337, 2006. Go to original source...
  59. Zhou, H., Konzak, C.F.: Improvement of anther culture methods for haploid production in wheat. - Crop Sci. 29: 817-821, 1989. Go to original source...
  60. Zhou, X., Wang, K., Lv, D., Wu, C., Li, J., Zhao, P., Lin, Z., Du, L., Yan, Y., Ye, X.: Global analysis of differentially expressed genes and proteins in the wheat callus infected by Agrobacterium tumefaciens. - PloS ONE 8: e79390, 2013. Go to original source...
  61. Ziegler, G., Dressler, K., Hess, D.: Investigations on the anther culturability of four German spring wheat cultivars and the influence of light on regeneration of green vs. albino plants. - Plant Breed. 105: 40-46, 1990. Go to original source...