OsSIG2A is required for chloroplast development in rice (Oryza sativa L.) at low temperature by regulating plastid genes expression
Yang Yu B * , Zhenling Zhou A * , Hanchun Pu A , Baoxiang Wang A , Yunhui Zhang B , Bo Yang A , Tongli Zhao A and Dayong Xu![https://orcid.org/0000-0003-4967-1596](/media/client/orcid_16x16.png)
A Lianyungang Academy of Agricultural Sciences, Lianyungang 222234, China.
B Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China.
C Corresponding author. Email: dayongxu3030@163.com
Functional Plant Biology 46(8) 766-776 https://doi.org/10.1071/FP18254
Submitted: 25 September 2018 Accepted: 26 March 2019 Published: 3 May 2019
Abstract
The chloroplast is an essential photosynthetic apparatus that is more sensitive to low temperatures than other organelles. Sigma factors were revealed regulating specific gene expression for maintaining photosynthetic efficiency and adapting to physiological and environmental conditions. However, the regulatory mechanisms of SIG genes supporting chloroplast development under low temperature in rice have not yet been reported. Here, we uncovered the essential role of OsSIG2A in rice chloroplast development at low temperatures by a newly reported thermo-sensitive chlorophyll deficient 12 (tcd12) mutant, which exhibited albino leaves with decreased chlorophyll content and malformed chloroplasts at seedling stage under low temperature. OsSIG2A is a typical chloroplast-localised RNA polymerase sigma factor, and constitutively expresses in different rice tissues, especially for young leaves and stems. Moreover, the transcription level of both PEP- and NEP- dependent genes, which are necessary for chloroplast development at early leaf development stage, was greatly affected in the tcd12 mutant under low temperature. Taken together, our findings indicate that OsSIG2A is required for early chloroplast differentiation under low temperatures by regulating plastid genes expression.
Additional keywords: chloroplast development, rice, RNA polymerase sigma factor, thermo-sensitive.
References
Allan DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science 6, 36–42.| Impacts of chilling temperatures on photosynthesis in warm-climate plants.Crossref | GoogleScholarGoogle Scholar |
Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
| Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 16654194PubMed |
Börner T, Aleynikova AY, Zubo YO, Kusnetsov VV (2015) Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochimica et Biophysica Acta 1847, 761–769.
| Chloroplast RNA polymerases: role in chloroplast biogenesis.Crossref | GoogleScholarGoogle Scholar | 25680513PubMed |
Chen S, Tao L, Zeng L, Vega-Sanchez ME, Umemura K, Wang GL (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Molecular Plant Pathology 7, 417–427.
| A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice.Crossref | GoogleScholarGoogle Scholar | 20507457PubMed |
Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Current Biology 6, 325–330.
| Engineered GFP as a vital reporter in plants.Crossref | GoogleScholarGoogle Scholar | 8805250PubMed |
Dong H, Fei GL, Wu CY, Wu FQ, Sun YY, Chen MJ, Ren YL, Zhou KN, Cheng ZJ, Wang JL, Jiang L, Zhang X, Guo XP, Lei CL, Su N, Wang H, Wan JM (2013) A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants. Plant Physiology 162, 1867–1880.
| A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants.Crossref | GoogleScholarGoogle Scholar | 23803583PubMed |
Ehlert B, Hincha DK (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods 4, 12
| Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 18505561PubMed |
Favory JJ, Kobayshi M, Tanaka K, Peltier G, Kreis M, Valay JG, Lerbs-Mache S (2005) Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Research 33, 5991–5999.
| Specific function of a plastid sigma factor for ndhF gene transcription.Crossref | GoogleScholarGoogle Scholar | 16243785PubMed |
Gong X, Su Q, Lin D, Jiang Q, Xu J, Zhang JH, Teng S, Dong Y (2014) The rice OsV4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress. Journal of Integrative Plant Biology 56, 400–410.
| The rice OsV4 encoding a novel pentatricopeptide repeat protein is required for chloroplast development during the early leaf stage under cold stress.Crossref | GoogleScholarGoogle Scholar | 24289830PubMed |
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. The EMBO Journal 16, 4041–4048.
| The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids.Crossref | GoogleScholarGoogle Scholar | 9233813PubMed |
Hanaoka M, Kanamaru K, Takahashi H, Tanaka K (2003) Molecular genetic analysis of chloroplast gene promoters dependent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase, in Arabidopsis thaliana. Nucleic Acids Research 31, 7090–7098.
| Molecular genetic analysis of chloroplast gene promoters dependent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase, in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 14654684PubMed |
Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Reports 6, 545–550.
| Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis.Crossref | GoogleScholarGoogle Scholar | 15877080PubMed |
Heber U, Shuvalov VA (2005) Photochemical reactions of chlorophyll in dehydrated photosystem II: two chlorophyll forms (680 and 700 nm). Photosynthesis Research 84, 85–91.
| Photochemical reactions of chlorophyll in dehydrated photosystem II: two chlorophyll forms (680 and 700 nm).Crossref | GoogleScholarGoogle Scholar | 16049759PubMed |
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. The Plant Journal 6, 271–282.
| Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA.Crossref | GoogleScholarGoogle Scholar | 7920717PubMed |
Hu F, Zhu Y, Wu W, Xie Y, Huang J (2015) Leaf variegation of Thylakoid Formation 1 is suppressed by mutations of specific σ-factors in Arabidopsis. Plant Physiology 168, 1066–1075.
| Leaf variegation of Thylakoid Formation 1 is suppressed by mutations of specific σ-factors in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25999408PubMed |
Ishizaki Y, Tsunoyama Y, Hatano K, Ando K, Shinmyo A, Kobori M, Takeba G, Nakahira Y, Shiina T (2005) A nulear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. The Plant Journal 42, 133–144.
| A nulear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons.Crossref | GoogleScholarGoogle Scholar | 15807777PubMed |
Jiang Q, Mei J, Gong XD, Xu JL, Zhang JH, Teng S, Lin DZ, Dong YJ (2014) Importance of the rice TCD9 encoding α subunit of chaperonin protein60 (Cpn60α) for the chloroplast development during the early leaf stage. Plant Science 215–216, 172–179.
| Importance of the rice TCD9 encoding α subunit of chaperonin protein60 (Cpn60α) for the chloroplast development during the early leaf stage.Crossref | GoogleScholarGoogle Scholar | 24388528PubMed |
Kanamaru K, Nagashima A, Fujiwara M, Shimada H, Shirano Y, Nakabayashi K, Shibata D, Tanaka K, Takahashi H (2001) An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant & Cell Physiology 42, 1034–1043.
| An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts.Crossref | GoogleScholarGoogle Scholar |
Kasai K, Kawagishi-Kobayashi M, Teraishi M, Ito Y, Ochi K, Wakasa K, Tozawa Y (2004) Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice. Bioscience, Biotechnology, and Biochemistry 68, 973–977.
| Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice.Crossref | GoogleScholarGoogle Scholar | 15118338PubMed |
Kusumi K, Iba K (2014) Establishment of the chloroplast genetic system in rice during early leaf development and at low temperatures. Frontiers in Plant Science 5, 386
| Establishment of the chloroplast genetic system in rice during early leaf development and at low temperatures.Crossref | GoogleScholarGoogle Scholar | 25157260PubMed |
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 Biotechnology 27, 85–90.
| Chloroplast biogenesis during the early stage of leaf development in rice.Crossref | GoogleScholarGoogle Scholar |
Kusumi K, Sakata C, Nakamura T, Kawasaki S, Yoshimura A, Iba K (2011) A plastid protein NUS1 is essential for build-up of the genetic system for early chloroplast development under cold stress conditions. The Plant Journal 68, 1039–1050.
| A plastid protein NUS1 is essential for build-up of the genetic system for early chloroplast development under cold stress conditions.Crossref | GoogleScholarGoogle Scholar | 21981410PubMed |
Lepage É, Zampini É, Brisson N (2013) Plastid genome instability leads to reactive oxygen species production and plastid-to-nucleus retrograde signaling in Arabidopsis. Plant Physiology 163, 867–881.
| Plastid genome instability leads to reactive oxygen species production and plastid-to-nucleus retrograde signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23969600PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Loschelder H, Schweer J, Link B, Link G (2006) Dual temporal role of plastid sigma factor 6 in Arabidopsis development. Plant Physiology 142, 642–650.
| Dual temporal role of plastid sigma factor 6 in Arabidopsis development.Crossref | GoogleScholarGoogle Scholar | 16905663PubMed |
Lysenko E (2006) Analysis of the evolution of the family of the Sig genes encoding plant sigma factor. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 53, 605–614.
| Analysis of the evolution of the family of the Sig genes encoding plant sigma factor.Crossref | GoogleScholarGoogle Scholar |
Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiology 103, 309
| Dynamic regulation of chloroplast transcription.Crossref | GoogleScholarGoogle Scholar | 8029331PubMed |
Nagashima A, Hanaoka M, Shikanai T, Fujiwara M, Kanamaru K, Takahashi H, Tanaka K (2004) The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light responsive promoter (BLRP) in Arabidopsis thaliana. Plant & Cell Physiology 45, 357–368.
| The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light responsive promoter (BLRP) in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Noordally ZB, Ishii K, Atkins KA, Wetherill SJ, Kusakina J, Walton EJ, Kato M, Azuma M, Tanaka K, Hanaoka M, Dodd AN (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339, 1316–1319.
| Circadian control of chloroplast transcription by a nuclear-encoded timing signal.Crossref | GoogleScholarGoogle Scholar | 23493713PubMed |
Peng X, Teng L, Yan X, Zhao M, Shen S (2015) The cold responsive mechanism of the paper mulberry: decreased photosynthesis capacity and increased starch accumulation. BMC Genomics 16, 898–917.
| The cold responsive mechanism of the paper mulberry: decreased photosynthesis capacity and increased starch accumulation.Crossref | GoogleScholarGoogle Scholar | 26537770PubMed |
Privat I, Hakimi MA, Buhot L, Favory JJ, Lerbs-Mache S (2003) Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3. Plant Molecular Biology 51, 385–399.
| Characterization of Arabidopsis plastid sigma-like transcription factors SIG1, SIG2 and SIG3.Crossref | GoogleScholarGoogle Scholar | 12602869PubMed |
Schweer J, Turkeri H, Kolpack A, Link G (2010) Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription – recent lessons from Arabidopsis thaliana. European Journal of Cell Biology 89, 940–946.
| Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription – recent lessons from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 20701995PubMed |
Song J, Wei XJ, Shao GN, Sheng ZH, Chen DB, Liu CL, Jiao GA, Xie LH, Tang SQ, Hu PS (2014) The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions. Plant Molecular Biology 84, 301–314.
| The rice nuclear gene WLP1 encoding a chloroplast ribosome L13 protein is needed for chloroplast development in rice grown under low temperature conditions.Crossref | GoogleScholarGoogle Scholar | 24132771PubMed |
Stoutjesdijk PA, Singh SP, Liu Q, Hurlstone CJ, Waterhouse PA, Green AG (2002) hpRNA-mediated targeting of the ArabidopsisFAD2 gene gives highly efficient and stable silencing. Plant Physiology 129, 1723–1731.
| hpRNA-mediated targeting of the ArabidopsisFAD2 gene gives highly efficient and stable silencing.Crossref | GoogleScholarGoogle Scholar | 12177485PubMed |
Sugimoto H, Kusumi K, Noguchi K, Yano M, Yoshimura A, Iba K (2007) The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria. The Plant Journal 52, 512–527.
| The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria.Crossref | GoogleScholarGoogle Scholar | 17727616PubMed |
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 24132122PubMed |
Tozawa Y, Teraishi M, Sasaki T, Sonoike K, Nishiyama Y, Itaya M, Miyao A, Hirochika H (2007) The plastid sigma factor SIG1 maintains photosystem I activity via regulated expression of the pasA operon in rice chloroplasts. The Plant Journal 52, 124–132.
| The plastid sigma factor SIG1 maintains photosystem I activity via regulated expression of the pasA operon in rice chloroplasts.Crossref | GoogleScholarGoogle Scholar | 17651366PubMed |
Tsunoyama Y, Morikawa K, Shiina T, Toyoshima Y (2002) Blue light specific and differential expression of a plastid sigma factor, Sig5 in Arabidopsis thaliana. FEBS Letters 516, 225–228.
| Blue light specific and differential expression of a plastid sigma factor, Sig5 in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 11959137PubMed |
Tsunoyama Y, Ishizaki Y, Morikawa K, Kobori M, Nakahira Y, Takeba G, Toshinori Y, Shiina T (2004) Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5. Proceedings of the National Academy of Sciences of the United States of America 101, 3304–3309.
| Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5.Crossref | GoogleScholarGoogle Scholar | 14976253PubMed |
Wang Y, Zhang J, Shi X, Peng Y, Li P, Lin D, Dong Y, Teng S (2016) Temperature-sensitive albino gene TCD5, encoding a monooxygenase, affects chloroplast development at low temperatures. Journal of Experimental Botany 67, 5187–5202.
| Temperature-sensitive albino gene TCD5, encoding a monooxygenase, affects chloroplast development at low temperatures.Crossref | GoogleScholarGoogle Scholar | 27531886PubMed |
Wang WJ, Zheng KL, Gong XD, Xu JL, Huang JR, Lin DZ, Dong YJ (2017) The rice TCD11 encoding plastid ribosomal protein S6 is essential for chloroplast development at low temperature. Plant Science 259, 1–11.
| The rice TCD11 encoding plastid ribosomal protein S6 is essential for chloroplast development at low temperature.Crossref | GoogleScholarGoogle Scholar | 28483049PubMed |
Wellburn AR (1994) The spectral determination of chlorophylls a and b as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
| The spectral determination of chlorophylls a and b as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar |
Woodson JD, Perez-Ruiz JM, Schmitz RJ, Ecker JR, Chory J (2013) Sigma factor-mediated plastid retrograde signals control nuclear gene expression. The Plant Journal 73, 1–13.
| Sigma factor-mediated plastid retrograde signals control nuclear gene expression.Crossref | GoogleScholarGoogle Scholar | 22950756PubMed |
Wu Z, Zhang X, He B, Diao L, Sheng S, Wang J, Guo X, Su N, Wang L, Jiang L, Wang C, Zhai H, Wan J (2007) A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiology 145, 29–40.
| A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar | 17535821PubMed |
Wu L, Wu J, Liu Y, Gong X, Xu J, Lin D, Dong Y (2016) The rice pentatricopeptide repeat gene TCD10 is needed for chloroplast development under cold stress. Rice 9, 67
| The rice pentatricopeptide repeat gene TCD10 is needed for chloroplast development under cold stress.Crossref | GoogleScholarGoogle Scholar | 27910002PubMed |
Yagi Y, Shiina T (2014) Recent advances in the study of chloroplast gene expression and its evolution. Frontiers in Plant Science 5, 61
| Recent advances in the study of chloroplast gene expression and its evolution.Crossref | GoogleScholarGoogle Scholar | 24611069PubMed |
Yamburenko MV, Zubo YO, Borner T (2015) Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: repression by guanosine-3′-5′-bisdiphosphate and activation by sigma factor 5. The Plant Journal 82, 1030–1041.
| Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: repression by guanosine-3′-5′-bisdiphosphate and activation by sigma factor 5.Crossref | GoogleScholarGoogle Scholar | 25976841PubMed |
Yao J, Roy-Chowdhury S, Allison LA (2003) AtSig5 is an essential nucleus-encoded Arabidopsis σ-like factor. Development and hormone action. Plant Physiology 132, 739–747.
| AtSig5 is an essential nucleus-encoded Arabidopsis σ-like factor. Development and hormone action.Crossref | GoogleScholarGoogle Scholar | 12805603PubMed |
Yoo SC, Cho SH, Sugimoto H, Li J, Kusumi K, Koh HJ, Iba K, Paek NC (2009) Rice virescent3 and stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development. Plant Physiology 150, 388–401.
| Rice virescent3 and stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development.Crossref | GoogleScholarGoogle Scholar | 19297585PubMed |
Yu QB, Huang C, Yang ZN (2014) Nuclear-encoded factors associated with the chloroplast transcription machinery of higher plants. Frontiers in Plant Science 5, 316
| Nuclear-encoded factors associated with the chloroplast transcription machinery of higher plants.Crossref | GoogleScholarGoogle Scholar | 25071799PubMed |
Zghidi W, Merendino L, Cottet A, Mache R, Lerbs-Mache S (2007) Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psb N gene in plastids. Nucleic Acids Research 35, 455–464.
| Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psb N gene in plastids.Crossref | GoogleScholarGoogle Scholar | 17175536PubMed |
Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994
| Sorting signals, N-terminal modifications and abundance of the chloroplast proteome.Crossref | GoogleScholarGoogle Scholar | 18431481PubMed |