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A naturally occurring conditional albino mutant in rice caused by defects in the plastid-localized OsABCI8 transporter

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Abstract

A wide range of molecules are transported across membranes by the ATP binding cassette (ABC) transporters. Plants possess a collection of ABC proteins bearing similarities to the components of prokaryotic multi subunit ABC transporters, designed as ABC group I. However the functions of most of them are not well understood. Here, we characterized a naturally occurring rice mutant that exhibited albino phenotype under continuous rainy days in the field, but gradually recovered to normal green after the rainy season. Molecular and genetic analyses revealed that the phenotypes were caused by a mutation in the OsABCI8 that encoded a member of the ABCI family. Subcellular localization demonstrated that OsABCI8 is a chloroplast ABC transporter. Expression of OsABCI8 is significantly enhanced in rainy days compared to sunny days. Besides defects in chloroplast development and chlorophyll biosynthesis, the mutant phenotype is accompanied by a higher accumulation of iron, suggesting that OsABCI8 is involved in iron transportation and/or homeostasis in rice. Our results demonstrate that OsABCI8 represents a conserved ABCI protein involved in transition metals transportation and/or homeostasis and suggest an important role of the plastid-localized OsABCI8 for chloroplast development.

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References

  • Cheng L, Wang F, Shou H, Huang F, Zheng L, He F, Li J, Zhao FJ, Ueno D, Ma JF, Wu P (2007) Mutation in nicotianamine aminotransferase stimulated the Fe(II) acquisition system and led to iron accumulation in rice. Plant Physiol 145:1647–1657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dei M (1985) Benzyladenine-induced stimulation of 5-aminolevulinic acid accumulation under various light intensities in levulinic acid-treated cotyledons of etiolated cucumber. Physiol Plant 64:153–160

    Article  CAS  Google Scholar 

  • Deng XJ, Zhang HQ, Wang Y, He F, Liu JL, Xiao X, Shu ZF, Li W, Wang GH, Wang GL (2014) Mapped clone and functional analysis of leaf-color gene Ygl7 in a rice hybrid (Oryza sativa L. ssp. indica). PLoS ONE 9:e99564

    Article  PubMed  PubMed Central  Google Scholar 

  • Duy D, Wanner G, Meda AR, von Wirén N, Soll J, Philippar K (2007) PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 19:986–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Gong X, Su Q, Lin D, Jiang Q, Xu J, Zhang J, 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. J Integr Plant Biol 56:400–410

    Article  CAS  PubMed  Google Scholar 

  • Grusak MA, Pezeshgi S (1996) Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiol 110:329–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi-Tsugane M, Takahara H, Ahmed N, Himi E, Takagi K, Iida S, Tsugane K, Maekawa M (2014) A mutable albino allele in rice reveals that formation of thylakoid membranes requires the SNOW-WHITE LEAF1 Gene. Plant Cell Physiol 55:3–15

    Article  CAS  PubMed  Google Scholar 

  • 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. Plant J 6:271–282

    Article  CAS  PubMed  Google Scholar 

  • Hodgins RR, Van Huystee RB (1986) Rapid simultaneous estimation of protoporphyrin and Mg-porphyrins in higher plants. J Plant Physiol 125:311–323

    Article  CAS  Google Scholar 

  • Ilag LL, Kumar AM, Söll D (1994) Light regulation of chlorophyll biosynthesis at the level of 5-aminolevulinate formation in Arabidopsis. Plant Cell 6:265–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML (2008) Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci U S A 105:10619–10624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 protein 60 (Cpn60α) for the chloroplast development during the early leaf stage. Plant Sci 215–216:172–179

    Article  PubMed  Google Scholar 

  • Jung K-H, Hur J, Ryu C-H, Choi Y, Chung Y-Y, Miyao A, Hirochika H, An G (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44:463–472

    Article  CAS  PubMed  Google Scholar 

  • Kusumi K, Iba K (2014) Establishment of the chloroplast genetic system in rice during early leaf development and at low temperatures. Front Plant Sci 5:386

    Article  PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK (1987) [34] Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol 148: 350–382

    Article  CAS  Google Scholar 

  • Massouh A, Schubert J, Yaneva-Roder L, Ulbricht-Jones ES, Zupok A, Johnson MTJ, Wright SI, Pellizzer T, Sobanski J, Bock R, Greiner S (2016) spontaneous chloroplast mutants mostly occur by replication slippage and show a biased pattern in the plastome of Oenothera. Plant Cell 28:911–929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moller SG, Kunkel T, Chua NH (2001) A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev 15:90–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuhaus HE, Emes MJ (2000) Non photosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140

    Article  CAS  PubMed  Google Scholar 

  • Nishida S, Tsuzuki C, Kato A, Aisu A, Yoshida J, Mizuno T (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442

    Article  CAS  PubMed  Google Scholar 

  • Peng L, Ma J, Chi W, Guo J, Zhu S, Lu Q, Lu C, Zhang L (2006) LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18:955–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W, Miyagishima S-y, Jarvis P (2008) Chloroplast biogenesis: control of plastid development, protein import, division and inheritance. Arabidopsis Book/Am Soc Plant Biol 6:e0110

    Google Scholar 

  • Shimoni-Shor E, Hassidim M, Yuval-Naeh N, Keren N (2010) Disruption of Nap14, a plastid-localized non-intrinsic ABC protein in Arabidopsis thaliana results in the over-accumulation of transition metals and in aberrant chloroplast structures. Plant Cell Environ 33:1029–1038

    Article  CAS  PubMed  Google Scholar 

  • Song J, Wei X, Shao G, Sheng Z, Chen D, Liu C, Jiao G, Xie L, Tang S, Hu P (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 Mol Biol 84:301–314

    Article  CAS  PubMed  Google Scholar 

  • Su N, Hu ML, Wu DX, Wu FQ, Fei GL, Lan Y, Chen XL, Shu XL, Zhang X, Guo XP, Cheng ZJ, Lei CL, Qi CK, Jiang L, Wang H, Wan JM (2012) Disruption of a rice pentatricopeptide repeat protein causes a seedling-specific albino phenotype and its utilization to enhance seed purity in hybrid rice production. Plant Physiol 159:227–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Wang W, Chen D, Ji Q, Jing Y, Wang H, Lin R (2012) Transposase-derived proteins FHY3/FAR1 interact with PHYTOCHROME-INTERACTING FACTOR1 to regulate chlorophyll biosynthesis by modulating HEMB1 during deetiolation in Arabidopsis. Plant Cell 24:1984–2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins–a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XM, Adams S, Chua NH, Moller SG (2004) AtNAP1 represents an atypical SufB protein in Arabidopsis plastids. J Biol Chem 280:6648–6654

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 Physiol 150:388–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Li C, Wu C, Xiong L, Chen G, Zhang Q, Wang S (2006) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34:D745–D748

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Su J, Duan S, Ao Y, Dai J, Liu J, Wang P, Li Y, Liu B, Feng D, Wang J, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant. Methods 7:30–30

    CAS  Google Scholar 

  • Zhou K, Ren Y, Lv J, Wang Y, Liu F, Zhou F, Zhao S, Chen S, Peng C, Zhang X, Guo X, Cheng Z, Wang J, Wu F, Jiang L, Wan J (2013) Young Leaf Chlorosis 1, a chloroplast-localized gene required for chlorophyll and lutein accumulation during early leaf development in rice. Planta 237:279–292

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the National Center of Plant Gene Research (Huazhong Agricultural University, China) for providing the T-DNA insertion line, ATL_03Z11JN90_LBT2, for the OsABCI8 gene. This work was supported by the National Natural Science Foundation of China (Grants Nos. 31671594 to XQ. Zhang and 31272491 to XM. Xie), the Natural Science Foundation of Anhui Province, China (Grant No. 1508085MC46 to B. Teng), Natural Science Foundation of Guangdong Province, China (Grant Nos. 2014A030313457 and 2015A020209118 to XQ. Zhang).

Author contributions

The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: XQZ TFH. Performed the experiments: XZ, RT, HG and SK. Analyzed the data: BT YHH XZ. Contributed reagents/materials/analysis tools: ZX XMX. Wrote the paper: XQZ TFH. All authors discussed the results and commented on the manuscript.

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Correspondence to Tzung-Fu Hsieh or Xiang-Qian Zhang.

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Xiuyu Zeng and Ran Tang have contributed equally to this work.

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Zeng, X., Tang, R., Guo, H. et al. A naturally occurring conditional albino mutant in rice caused by defects in the plastid-localized OsABCI8 transporter. Plant Mol Biol 94, 137–148 (2017). https://doi.org/10.1007/s11103-017-0598-4

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