Abstract
Although much information regarding the chloroplast and chromoplast biosynthesis has been accumulated in recent years, details of the physiological, biochemical, and molecular differences between green tissues and colorful chromoplast tissues are still poorly understood. In this study, the pigment accumulation, plastid ultrastructure, and the expression of genes involved in chloroplast synthesis were analyzed between leaf and corolla in cabbage and rapeseed. The results showed that both petals contained less chlorophyll contents and a lower ratio of Chl a/b, but contained higher carotenoid contents compared with that of sepals and leaves. Accordingly, ultrastructural observations indicated that plastid development of petals was arrested or inhibited. In addition, data obtained from biochemical studies were correlated with those at the mRNA level, the transcripts of almost all the chlorophyll biosynthetic genes (especially the downstream genes) and plastid genes required for early chloroplast development and photosynthesis were higher in leaves than that in petals. Besides, the different pigment accumulation in corollas was also corroborated by the changes in the expression of selected genes associated with chlorophyll accumulation and/or chloroplast development. Collectively, the results contribute to better understand the molecular mechanisms underlying tissue-specific chloroplast development in plants.
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References
Aschan G, Pfanz H (2003) Non-foliar photosynthesis–a strategy of additional carbon acquisition. Flora Morphol Distrib Funct Ecol Plants 198(2):81–97
Aschan G, Pfanz H, Vodnik D, Batič F (2005) Photosynthetic performance of vegetative and reproductive structures of green hellebore (Helleborus viridis L. agg.). Photosynthetica 43(1):55–64
Bang WY, Chen J, Jeong IS, Kim SW, Kim CW, Jung HS, Lee KH, Kweon H-S, Yoko I, Shiina T, Bahk JD (2012) Functional characterization of ObgC in ribosome biogenesis during chloroplast development. Plant J 71(1):122–134
Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89(3):1011–1018
Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60(1):43–73
Beale SI (2005) Green genes gleaned. Trends Plant Sci 10(7):309–312
Börner T, Aleynikova AY, Yan OZ, Kusnetsov VV (2015) Chloroplast RNA polymerases: Role in chloroplast biogenesis. Biochimica et Biophysica Acta (BBA) Bioenergetics 1847(9):761–769
Brzezowski P, Schlicke H, Richter A, Dent RM, Niyogi KK, Grimm B (2014) The GUN4 protein plays a regulatory role in tetrapyrrole biosynthesis and chloroplast-to-nucleus signalling in Chlamydomonas reinhardtii. Plant J Cell Amp Mol Biol 79(2):285–298
Dong C, Shao L, Liu G, Wang M, Liu H, Xie B, Li B, Fu Y, Liu H (2015) Photosynthetic characteristics, antioxidant capacity and biomass yield of wheat exposed to intermittent light irradiation with millisecond-scale periods. J Plant Physiol 184:28–36
Eckhardt U, Grimm B, H rtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56(1):1–14
Egea I, Barsan C, Bian W, Purgatto E, Latché A, Chervin C, Bouzayen M, Pech J-C (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51(10):1601–1611
Estévez JM, Cantero A, Romero C, Kawaide H, Jiménez LF, Kuzuyama T, Seto H, Kamiya Y, León P (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-d-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124(1):95–104
Hajdukiewicz PT, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16(13):4041–4048
Hills AC, Khan S, López-Juez E (2015) Chloroplast biogenesis-associated nuclear genes: control by plastid signals evolved prior to their regulation as part of photomorphogenesis. Front Plant Sci 6:1078
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217(2–3):185–194
Keck RW, Dilley RA, Allen CF, Biggs S (1970) Chloroplast composition and structure differences in a soybean mutant. Plant Physiol 46(5):692–698
Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316(5825):715–719
Kusumi K, Chono Y, Shimada H, Gotoh E, Tsuyama M, Iba K (2010) Chloroplast biogenesis during the early stage of leaf development in rice. Plant Biotechnol 27(1):85–90
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Sci Signal 299(5608):902
Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RM (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 31(2):171–188
Lieberman M, Segev O, Gilboa N, Lalazar A, Levin I (2004) The tomato homolog of the gene encoding UV-damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. TAG Theor Appl Genet 108(8):1574–1581
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time puantitative PCR and the 2−∆∆CT method. Methods 25(4):402–408
Lopez AB, Van Eck J, Conlin BJ, Paolillo DJ, O’Neill J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59(2):213–223
Lu S, Van Eck J, Zhou X, Lopez AB, O’Halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell 18(12):3594–3605
Ma L, Sun N, Liu X, Jiao Y, Zhao H, Deng XW (2005) Organ-specific expression of Arabidopsis genome during development. Plant Physiol 138(1):80–91
Marano MR, Serra EC, Orellano EG, Carrillo N (1993) The path of chromoplast development in fruits and flowers. Plant science 94(1):1–17
Mullet JE (1988) Chloroplast development and gene expression. Ann Rev Plant Physiol Plant Mol Biol 39(1):475–502
Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103(2):309–313
Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11(2):145–157
Nakamura H, Muramatsu M, Hakata M, Ueno O, Nagamura Y, Hirochika H, Takano M, Ichikawa H (2009) Ectopic overexpression of the transcription factor OsGLK1 induces chloroplast development in non-green rice cells. Plant cell physiol 50(11):1933–1949
Nott A, Jung H-S, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759
Pfalz J, Pfannschmidt T (2013) Essential nucleoid proteins in early chloroplast development. Trends Plant Sci 18(4):186–194
Qi J, Yu S, Zhang F, Shen X, Zhao X, Yu Y, Zhang D (2010) Reference gene selection for real-time quantitative polymerase chain reaction of mRNA transcript levels in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Mol Biology Report 28(4):597–604
Qiao J, Ma C, Wimmelbacher M, Börnke F, Luo M (2011) Two novel proteins, MRL7 and its paralog MRL7-L, have essential but functionally distinct roles in chloroplast development and are involved in plastid gene expression regulation in Arabidopsis. Plant Cell Physiol 52(6):1017–1030
Rochaix JD, Ramundo S (2015) Conditional repression of essential chloroplast genes: evidence for new plastid signaling pathways. Biochim Et Biophys Acta 1847(9):986–992
Salopek-Sondi B, Magnus V (2007) Developmental studies in the Christmas rose (Helleborus niger L.). Int J Plant Dev Biol 1:151–159
Sasaki K, Takahashi T (2002) A flavonoid from Brassica rapa flower as the UV-absorbing nectar guide. Phytochemistry 61(3):339–343
Schroeder DF, Gahrtz M, Maxwell BB, Cook RK, Kan JM, Alonso JM, Ecker JR, Chory J (2002) De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr Biol 12(17):1462–1472
Vainstein A, Sharon R (1993) Biogenesis of petunia and carnation corolla chloroplasts: changes in the abundance of nuclear and plastid-encoded photosynthesis-specific gene products during flower development. Physiol Plant 89(1):192–198
Vemmos S, Goldwin G (1993) Stomatal and chlorophyll distribution of Cox’s Orange Pippin apple flowers relative to other cluster parts. Ann Bot (Lond) 71(3):245–250
Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim et Biophys Acta (BBA) Mol Cell Res 1541(1):91–101
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307–313
Yu QB, Jiang Y, Chong K, Yang ZN (2009) AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J 59:1011–1023
Zhao C, Xu J, Chen Y, Mao C, Zhang S, Bai Y, Jiang D, Wu P (2012) Molecular cloning and characterization of OsCHR4, a rice chromatin-remodeling factor required for early chloroplast development in adaxial mesophyll. Planta 236(4):1165–1176
Zhao S, Long W, Wang Y, Liu L, Wang Y, Niu M, Zheng M, Wang D, Wan J (2016) A rice White-stripe leaf3 (wsl3) mutant lacking an HD domain-containing protein affects chlorophyll biosynthesis and chloroplast development. J Plant Biol 59(3):282–292
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The authors thank all laboratory members for help, advice and discussion. This work was supported by National Natural Science Foundation of China (No. 31572129), and the Natural Science Foundation of Chongqing of China (cstc2015jcyjA80026), and the Fundamental Research Funds for the Central Universities (No. 106112015CDJZR235504).
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M. Zhu and X. Meng have contributed equally to this work.
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Zhu, M., Meng, X., Chen, G. et al. Physiological, biochemical, and molecular differences in chloroplast synthesis between leaf and corolla of cabbage (Brassica rapa L. var. chinensis) and rapeseed (Brassica napus L.). Plant Growth Regul 82, 91–101 (2017). https://doi.org/10.1007/s10725-016-0241-4
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DOI: https://doi.org/10.1007/s10725-016-0241-4