Plant Growth Regulation

, Volume 84, Issue 2, pp 249–260 | Cite as

OsSLA4 encodes a pentatricopeptide repeat protein essential for early chloroplast development and seedling growth in rice

  • Zhong-wei Wang
  • Jun Lv
  • Shu-zhang Xie
  • Yu Zhang
  • Zhen-nan Qiu
  • Ping Chen
  • Yong-tao Cui
  • Yao-fang Niu
  • Shi-kai Hu
  • Hong-zhen Jiang
  • Sheng-zhen Ge
  • HaiPhuong Trinh
  • Kai-rong Lei
  • Wen-qin Bai
  • Yi Zhang
  • Long-biao Guo
  • De-yong Ren
Original paper
  • 148 Downloads

Abstract

In land plants, chloroplast transcripts undergo post-transcriptional modifications, including splicing, editing, trimming, etc., before translation, and a set of nuclear-encoded proteins regulate this essential step. In this study, we characterized a rice (Oryza sativa) seedling-lethal albino mutant sla4 from the progeny of tissue culture plants of the japonica cultivar Zhonghua 11. The sla4 mutant exhibited an albino phenotype from germination through the third-leaf stage, and then gradually died. The sla4 mutants lacked photosynthetic pigments and had severe defects in photosynthesis and early chloroplast development. Map-based cloning showed that a 13-bp deletion in the coding region of OsSLA4 on chromosome 7 resulted in the albino phenotype and albino mutants were also generated by knocking-out OsSLA4 in wild type with the CRISPR/Cas9 system. OsSLA4 encodes a chloroplast-localized pentatricopeptide repeat (PPR) protein with 15 PPR motifs and an atypical DYW-like motif. Loss-of-function of OsSLA4 resulted in severe defects in the intron splicing of atpF, ndhA, petB, rpl2, rpl16, rps12-2, and trnG, as well as a significant reduction in the transcript levels of chloroplast ribosomal RNAs and some chloroplast development- and photosynthesis-related genes. These results indicate that OsSLA4 is indispensable for early chloroplast development and seedling growth in rice, most likely acting by influencing the intron splicing of multiple chloroplast group II introns.

Keywords

Oryza sativa Seedling-lethal albino Pentatricopeptide repeat protein Intron splicing Chloroplast development 

Notes

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant Nos. 31701390, 31461143014, 31661143006, 91535205), the National Key Research and Development Program of China (Grant No. 2016YFD0100902-07), Zhejiang Provincial Natural Science Foundation of China (Grant No. LY18C130007).

Compliance with ethical standards

Conflict of interest

The authors declare no potential competing interests.

Supplementary material

10725_2017_336_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1101 KB)

References

  1. Aryamanesh N, Ruwe H, Sanglard LVP, Eshraghi L, Bussell JD, Howell KA, Small ID, Francs-Small CC (2017) The pentatricopeptide repeat protein EMB2654 is essential for trans-splicing of a chloroplast small ribosomal subunit transcript. Plant Physiol 173:1164–1176CrossRefPubMedGoogle Scholar
  2. Asakura Y, Bayraktar OA, Barkan A (2008) Two CRM protein subfamilies cooperate in the splicing of group IIB introns in chloroplasts. RNA 14:2319–2332CrossRefPubMedPubMedCentralGoogle Scholar
  3. Asano T, Miyao A, Hirochika H, Kikuchi S, Kadowaki K (2013) A pentatricopeptide repeat gene of rice is required for splicing of chloroplast transcripts and RNA editing of ndhA. Plant Biotechnol 30:57–64CrossRefGoogle Scholar
  4. Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442CrossRefPubMedGoogle Scholar
  5. Corneille S, Lutz K, Maliga P (2000) Conservation of RNA editing between rice and maize plastids: are most editing events dispensable? Mol Gen Genet 264:419–424CrossRefPubMedGoogle Scholar
  6. Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221:424–436CrossRefPubMedGoogle Scholar
  7. de Longevialle AF, Small ID, Lurin C (2010) Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol Plant 3:691–705CrossRefPubMedGoogle Scholar
  8. Forsthoefel NR, Wu YW, Schulz B, Bennett MJ, Feldmann KA (1992) T-DNA insertion mutagenesis in Arabidopsis : prospects and perspectives. Aust J Plant Physiol 19:353–366CrossRefGoogle Scholar
  9. Fujii S, Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol 191:37–47CrossRefPubMedGoogle Scholar
  10. Germain A, Hotto AM, Barkan A, Stern DB (2013) RNA processing and decay in plastids. Wires RNA 4:295–316CrossRefPubMedGoogle Scholar
  11. Gothandam KM, Kim ES, Cho HJ, Chung YY (2005) OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis. Plant Mol Biol 58:421–433CrossRefPubMedGoogle Scholar
  12. Hajdukiewicz PTJ, 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 16:4041–4048CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hammani K, Barkan A (2014) An mTERF domain protein functions in group II intron splicing in maize chloroplasts. Nucleic Acids Res 42:5033–5042CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hammani K, Takenaka M, Miranda R, Barkan A (2016) A PPR protein in the PLS subfamily stabilizes the 5′-end of processed rpl16 mRNAs in maize chloroplasts. Nucleic Acids Res 44:4278–4288CrossRefPubMedPubMedCentralGoogle Scholar
  15. Harris EH, Boynton JE, Gillham NW (1994) Chloroplast ribosomes and protein synthesis. Microbiol Rev 58:700–754PubMedPubMedCentralGoogle Scholar
  16. Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J 36:541–549CrossRefPubMedGoogle Scholar
  17. Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3:824–834CrossRefPubMedGoogle Scholar
  18. Inada M, Sasaki T, Yukawa M, Tsudzuki T, Sugiura M (2004) A systematic search for RNA editing sites in pea chloroplasts: an editing event causes diversification from the evolutionarily conserved amino acid sequence. Plant Cell Physiol 45:1615–1622CrossRefPubMedGoogle Scholar
  19. Jarvis P, Lopez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802CrossRefPubMedGoogle Scholar
  20. Jenkins BD, Barkan A (2001) Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J 20:872–879CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jenkins BD, Kulhanek DJ, Barkan A (1997) Nuclear mutations that block group II RNA splicing in maize chloroplasts reveal several intron classes with distinct requirements for splicing factors. Plant Cell 9:283–296CrossRefPubMedPubMedCentralGoogle Scholar
  22. Khrouchtchova A, Monde RA, Barkan A (2012) A short PPR protein required for the splicing of specific group II introns in angiosperm chloroplasts. RNA 18:1197–1209CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  24. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382CrossRefGoogle Scholar
  25. Liere K, Börner T (2007) Transcription and transcriptional regulation in plastids. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin, pp 121–174CrossRefGoogle Scholar
  26. Lin DZ, Gong XD, Jiang Q, Zheng KL, Zhou H, Xu JL, Teng S, Dong YJ (2015) The rice ALS3 encoding a novel pentatricopeptide repeat protein is required for chloroplast development and seedling growth. Rice 8:17CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu WZ, Fu YP, Hu GC, Si HM, Zhu L, Wu C, Sun ZX (2007) Identification and fine mapping of a thermo-sensitive chlorophyll deficient mutant in rice (Oryza sativa L.). Planta 226:785–795CrossRefPubMedGoogle Scholar
  28. Liu C, Zhu H, Xing Y, Tan J, Chen X, Zhang J, Peng H, Xie Q, Zhang Z (2016) Albino Leaf 2 is involved in the splicing of chloroplast group I and II introns in rice. J Exp Bot 67:5339–5347CrossRefPubMedPubMedCentralGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2– ∆∆CT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  30. Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Ret ML, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ma XL, Zhang QY, Zhu QL, Liu W, Chen Y, Qiu R, Wang B, Yang ZF, Li HY, Lin YR, Xie YY, Shen RX, Chen SF, Wang Z, Chen YL, Guo JX, Chen LT, Zhao XC, Dong ZC, Liu YG (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284CrossRefPubMedGoogle Scholar
  32. Marin-Navarro J, Manuell AL, Wu J, Mayfield SP (2007) Chloroplast translation regulation. Photosynth Res 94:359–374CrossRefPubMedGoogle Scholar
  33. Michel F, Kazuhiko U, Haruo O (1989) Comparative and functional anatomy of group II catalytic introns-a review. Gene 82:5–30CrossRefPubMedGoogle Scholar
  34. Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Phys 51:111–140CrossRefGoogle Scholar
  35. O’Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25:1120–1128CrossRefPubMedGoogle Scholar
  36. Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell 21:146–156CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ostheimer GJ, Williams-Carrier R, Belcher S, Osborne E, Gierke J, Barkan A (2003) Group II intron splicing factors derived by diversification of an ancient RNA-binding domain. EMBO J 22:3919–3929CrossRefPubMedPubMedCentralGoogle Scholar
  38. Schallenberg-Rudinger M, Knoop V (2016) Coevolution of organelle RNA editing and nuclear specificity factors in early land plants. Adv Bot Res 78:37–93CrossRefGoogle Scholar
  39. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650–2663CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shen YJ, Jiang H, Jin JP, Zhang ZB, Xi B, He YY, Wang G, Wang C, Qian L, Li X, Yu QB, Liu HJ, Chen DH, Gao JH, Huang H, Shi TL, Yang ZN (2004) Development of genome-wide DNA polymorphism database for map-based cloning of rice genes. Plant Physiol 135:1198–1205CrossRefPubMedPubMedCentralGoogle Scholar
  41. Small ID, Peeters N (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25:46–47CrossRefPubMedGoogle Scholar
  42. Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61:125–155CrossRefPubMedGoogle Scholar
  43. Sun HZ, Peng T, Zhang J, Li JZ, Du YX, Zhao QZ (2017) Test of small RNA sequencing repeatability in rice. Rice Sci 24:56–60CrossRefGoogle Scholar
  44. Tan JJ, Tan ZH, Wu FQ, Sheng PK, Heng YQ, Wang XH, Ren YL, Wang JL, Guo XP, Zhang X, Cheng ZJ, Jiang L, Liu XN, Wang HY, Wan JM (2014) A novel chloroplast-localized pentatricopeptide repeat protein involved in splicing affects chloroplast development and abiotic stress response in rice. Mol Plant 7:1329–1349CrossRefPubMedGoogle Scholar
  45. Till B, Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2001) CRS1 is a novel group II intron splicing factor that was derived from a domain of ancient origin. RNA 7:1227–1238CrossRefPubMedPubMedCentralGoogle Scholar
  46. Toda T, Fujii S, Noguchi K, Kazama T, Toriyama K (2012) Rice MPR25 encodes a pentatricopeptide repeat protein and is essential for RNA editing of nad5 transcripts in mitochondria. Plant J 72:450–460CrossRefPubMedGoogle Scholar
  47. Wang JL, Jiang JD, Oard JH (2000) Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.). Plant Sci 156:201–211CrossRefPubMedGoogle Scholar
  48. Wang DK, Liu HQ, Zhai GW, Wang LS, Shao JF, Tao YZ (2016a) OspTAC2 encodes a pentatricopeptide repeat protein and regulates rice chloroplast development. J Genet Genom 43:601–608CrossRefGoogle Scholar
  49. Wang L, Xu J, Nian JQ, Shen NW, Lai KK, Hu J, Zeng DL, Ge CW, Fang YX, Zhu L, Qian Q, Zhang GH (2016b) Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development. Plant Growth Regul 78:345–356CrossRefGoogle Scholar
  50. Wang ZW, Zhang TQ, Xing YD, Zeng XQ, Wang L, Liu ZX, Shi JQ, Zhu XY, Ma L, Li YF, Ling YH, Sang XC, He GH (2016c) YGL9, encoding the putative chloroplast signal recognition particle 43 kDa protein in rice, is involved in chloroplast development. J Integr Agric 15:944–953CrossRefGoogle Scholar
  51. Watkins KP, Kroeger TS, Cooke AM, Williams-Carrier RE, Friso G, Belcher SE, van Wijk KJ, Barkan A (2007) A ribonuclease III domain protein functions in group II intron splicing in maize chloroplasts. Plant Cell 19:2606–2623CrossRefPubMedPubMedCentralGoogle Scholar
  52. Williams PM, Barkan A (2003) A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J 36:675–686CrossRefPubMedGoogle Scholar
  53. Xie KB, Minkenberg B, Yang YN (2015) Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA 112:3570–3575CrossRefPubMedPubMedCentralGoogle Scholar
  54. Xu X, Zhang XB, Shi YF, Wang HM, Feng BH, Li XH, Huang QN, Song LX, Guo D, He Y, Wu JL (2016) A point mutation in an F-box domain-containing protein is responsible for brown hull phenotype in rice. Rice Sci 23:1–8CrossRefGoogle Scholar
  55. Yap A, Kindgren P, des Francs-Small CC, Kazama T, Tanz SK, Toriyama K, Small I (2015) AEF1/MPR25 is implicated in RNA editing of plastid atpF and mitochondrial nad5, and also promotes atpF splicing in Arabidopsis and rice. Plant J 81:661–669CrossRefPubMedGoogle Scholar
  56. Ye JW, Gong ZY, Chen CG, Mi HL, Chen GY (2012) A mutation of OSOTP 51 leads to impairment of photosystem I complex assembly and serious photo-damage in rice. J Integr Plant Biol 54:87–98CrossRefPubMedGoogle Scholar
  57. Yu HP, Qiu ZN, Xu QK, Wang ZW, Zeng DL, Hu J, Zhang GH, Zhu L, Gao ZY, Cheng G, Guo LB, Qian Q, Ren DY (2017) Fine mapping of LOW TILLER 1, a gene controlling tillering and panicle branching in rice. Plant Growth Regul 83:93–104CrossRefGoogle Scholar
  58. Zhang Y, Su JB, Duan S, Ao Y, Dai JR, Liu J, Wang P, Li YG, Liu B, Feng DR, Wang JF, Wang HB (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7:30CrossRefPubMedPubMedCentralGoogle Scholar
  59. Zhang ZG, Cui XA, Wang YW, Wu JX, Gu XF, Lu TG (2017) The RNA editing factor WSP1 is essential for chloroplast development in rice. Mol Plant 10:86–98CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Zhong-wei Wang
    • 1
    • 2
  • Jun Lv
    • 3
  • Shu-zhang Xie
    • 2
  • Yu Zhang
    • 1
  • Zhen-nan Qiu
    • 1
  • Ping Chen
    • 1
  • Yong-tao Cui
    • 1
  • Yao-fang Niu
    • 1
  • Shi-kai Hu
    • 1
  • Hong-zhen Jiang
    • 1
  • Sheng-zhen Ge
    • 3
  • HaiPhuong Trinh
    • 3
  • Kai-rong Lei
    • 2
  • Wen-qin Bai
    • 2
  • Yi Zhang
    • 3
  • Long-biao Guo
    • 1
  • De-yong Ren
    • 1
  1. 1.State Key Lab of Rice BiologyChina National Rice Research InstituteZhejiangChina
  2. 2.Biotechnology Research CenterChongqing Academy of Agricultural SciencesChongqingChina
  3. 3.Southwest UniversityChongqingChina

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