A novel RNA binding protein affects rbcL gene expression and is specific to bundle sheath chloroplasts in C4 plants

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Bowman, Shaun M ^a,b   Patel, Minesh ^a,c   Yerramsetty, Pradeep ^a   Mure, Christopher M ^a   Zielinski, Amy M ^a   Bruenn, Jeremy A ^a   Berry, James O ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b Clarke College   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

C3 Arabidopsis; C4 maize; C4 photosynthesis; Cell type specificity; Post transcriptional control; RbcL gene expression; S1 domain RNA binding protein

Indexed keywords

ARABIDOPSIS; ZEA MAYS;

RNA BINDING PROTEIN; VEGETABLE PROTEIN;

ARTICLE; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; MAIZE; MESOPHYLL CELL; METABOLISM; PHOTOSYNTHESIS; PLANT LEAF;

CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; MESOPHYLL CELLS; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; RNA-BINDING PROTEINS; ZEA MAYS;

EID: 84884331858     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-138     Document Type: Article

References (99)

1. Raghavendra AS, Sage RF. Introduction. C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, Volume 32 2011, 17-25. The Netherlands: Springer Dordrecht, Raghavendra AS, Sage RF.
2. Sage RF, Zhu X-G. Exploiting the engine of C4 photosynthesis. J Exp Bot 2011, 62:2989-3000. 10.1093/jxb/err179, 21652533.
3. Sage RF, Sage TL, Kocacinar F. Photorespiration and the evolution of C4 photosynthesis. Ann Rev Plant Biol 2012, 63:19-47.
4. Jones MB. C4 species as energy crops. C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, Volume 32 2011, 379-397. The Netherlands: Springer Dordrecht, Raghavendra AS, Sage RF.
5. Berry JO, Zielinski AM, Patel M. Gene expression in mesophyll and bundle sheath cells of C4 plants. C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, Volume 32 2011, 221-256. The Netherlands: Springer Dordrecht, Raghavendra AS, Sage RF.
6. Berry JO, Yerramsetty P, Zielinski AM, Mure C. Photosynthetic gene expression in higher plants. Photosyn Res 2013, doi:10.1007/s11120-013-9880-8.
7. Patel M, Berry JO. Rubisco gene expression in C4 plants. J Exp Bot 2008, 59:1625-1634.
8. von Caemmerer S, Furbank RT. The C4 pathway: an efficient CO2 pump. Photosyn Res 2003, 77:191-207. 10.1023/A:1025830019591, 16228376.
9. Hatch MD. C4 photosynthesis: a unique blend of modified biochemistry, anatomy, and ultrastructure. Biochem Biophys Acta 1987, 895:81-106.
10. Edwards GE, Voznesenskaya EV. C4 photosynthesis: Kranz forms and single-cell C4 in terretrial plants. C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, Volume 32 2011, 29-61. The Netherlands: Springer Dordrecht, Raghavendra AS, Sage RF.
11. Hibberd JM, Covshoff S. The regulation of gene expression required for C4 photosynthesis. Ann Rev Plant Biol 2010, 61:181-207.
12. Langdale J. C4 Cycles: past, present, and future research on C4 photosynthesis. Plant Cell 2011, 23:3879-3892. 10.1105/tpc.111.092098, 3246324, 22128120.
13. Tyagi AK, Gaur T. Light regulation of nuclear photosynthetic genes in higher plants. Crit Rev Plant Sci 2003, 22:417-452.
14. Raynaud C, Loisela C, Wostrikoff K, Kuras R, Girard-Bascou J, Wollman FA, Choquet Y. Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast. Proc Natl Acad Sci U S A 2007, 104:9093-9098. 10.1073/pnas.0703162104, 1885633, 17494733.
15. Johnson X, Wostrikoff K, Finazzi G, Kuras R, Schwarz C, Bujaldon S, Nickelsen J, Stern DB, Wollman F-A, Vallon O. MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 2010, 22:234-248. 10.1105/tpc.109.066266, 2828700, 20097872.
16. Tillich M, Beick S, Schmitz-Linneweber C. Chloroplast RNA-binding proteins: repair and regulation of chloroplast transcripts. RNA Biol 2010, 7:172-178. 10.4161/rna.7.2.11090, 20215878.
17. Barkan A. Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 2011, 155:1520-1532. 10.1104/pp.110.171231, 3091090, 21346173.
18. Slewinski TL, Anderson AA, Zhang C, Turgeon R. Scarecrow plays a role in establishing kranz anatomy in maize leaves. Plant Cell Physiol 2013, 53:2030-2037.
19. Gutteridge S, Gatenby AA. Rubisco synthesis, assembly, mechanism, and regulation. Plant Cell 1995, 7:809-819. 160870, 12242387.
20. Rodermel S. Subunit control of Rubisco biosynthesis - a relic of an endosymbiotic past?. Photosyn Res 1999, 59:105-123.
21. Wostrikoff K, Clark A, Sato S, Clemente T, Stern D. Ectopic expression of rubisco subunits in maize mesophyll cells does not overcome barriers to cell type-specific accumulation. Plant Physiol 2012, 160:419-432. 10.1104/pp.112.195677, 3440216, 22744982.
22. Brown NJ, Newell CA, Stanley S, Chen JE, Perrin AJ, Kajala K, Hibberd JM. Independent and parallel recruitment of pre-existing mechanisms underlying C4 photosynthesis. Science 2011, 331:1436-1439. 10.1126/science.1201248, 21415351.
23. Manuell A, Beligni MV, Yamaguchi K, Mayfield SP. Regulation of chloroplast translation: interactions of RNA elements, RNA-binding proteins and the plastid ribosome. Biochem Soc Trans 2004, 32:601-605. 10.1042/BST0320601, 15270686.
24. Stern DB, Goldschmidt-Clermont M, Hanson MR. Chloroplast RNA metabolism. Annu Rev Plant Biol 2010, 61:125-155. 10.1146/annurev-arplant-042809-112242, 20192740.
25. Schmitz-Linneweber C, Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 2008, 13:663-670. 10.1016/j.tplants.2008.10.001, 19004664.
26. McCormac DJ, Litz H, Wang J, Gollnick PD, Berry JO. Light-associated and processing-dependent protein binding to the 5′ UTR of rbcL mRNA in the chloroplasts of a C4 plant. J Biol Chem 2001, 276:3476-3483. 10.1074/jbc.M009236200, 11076953.
27. Yao W, Muqtadir K, Bruenn JA. Packaging in a yeast double-stranded RNA virus. J Virol 1995, 69:1917-1919. 188807, 7853534.
28. Maai E, Miyake H, Taniguchi M. Differential positioning of chloroplasts in C4 mesophyll and bundle sheath cells. Plant Signal Behav 2011, 6:111-113.
29. Covshoff S, Furbank RT, Leegood RC, Hibberd JM. Leaf rolling allows quantification of mRNA abundance in mesophyll cells of sorghum. J Exp Bot 2012, 64:807-813.
30. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeion R, Liu P, Sun Q, Nelson T, Brutnell TP. The developmental dynamics of the maize leaf transcriptome. Nature Genet 2010, 42:1060-1067. 10.1038/ng.703, 21037569.
31. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, Turgeon R, Wijk KJ. Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 2010, 22:3509-3542. 10.1105/tpc.110.079764, 3015116, 21081695.
32. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326:1112-1115. 10.1126/science.1178534, 19965430.
33. Chang YM, Liu WY, Shih AC, Shen MN, Lu CH, Lu MY, Yang HW, Wang TY, Chen SC, Chen SM, Li WH, Ku MS. Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol 2002, 160:165-177.
34. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Morales DR, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009, 106:11667-11672. 10.1073/pnas.0904715106, 2704857, 19571010.
35. Selth LA, Gilbert C, Svejstrup JQ. RNA immunoprecipitation to determine RNA-protein associations in vivo. Cold Spring Harb Protoc 2009, pdb.prot5234. doi:10.1101/pdb.prot5234.
36. Steeves TA, Sussex IM. Patterns in Plant Development 1989, Cambridge: Cambridge University Press.
37. Sylvester AW, Cande WZ, Freeling M. Division and differentiation during normal and liguleless-1 maize leaf development. Development 1990, 110:985-1000.
38. Barkan A. Nuclear mutants of maize with defects in chloroplast polysome assembly have altered chloroplast RNA metabolism. Plant Cell 1993, 5:389-402. 160279, 12271069.
39. Sheen J-Y, Bogorad L. Differential expression of genes for photosystem II components encoded by the plastid genome in bundle sheath and mesophyll cells of maize. Plant Physiol 1988, 86:1020-1026. 10.1104/pp.86.4.1020, 1054621, 16666025.
40. Li Y, Sugiura M. Three distinct ribonucleoproteins from tobacco chloroplasts: each contains a unique amino terminal acidic domain and two ribonucleoprotein consensus motifs. EMBO J 1990, 9:3059-3066. 552030, 1698606.
41. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, Miller N, Mueller LA, Mundodi S, Reiser L, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P. The Arabidopsis information resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nuc Acids Res 2003, 31:224-228.
42. Hetherington SE, Smillie RM, Davies WJ. Photosynthetic activities of vegetative and fruiting tissues of tomato. J Exp Bot 1999, 49:1173-1181.
43. Pyke K. Mesophyll. eLS 2012, doi:10.1002/9780470015902.a0002081.pub2.
44. Bycroft M, Hubbard TJP, Proctor M, Freund SMV, Murzin AG. The solution structure of the S1 RNA binding domain: A member of an ancient nucleic acid-binding fold. Cell 1997, 88:235-242. 10.1016/S0092-8674(00)81844-9, 9008164.
45. Yehudai-Resheff S, Portnoy V, Yogev S, Adir N, Schuster G. Domain analysis of the chloroplast polynucleotide phosphorylase reveals discrete functions in RNA degradation, polyadenylation, and sequence homology with exosome proteins. Plant Cell 2003, 15:2003-2019. 10.1105/tpc.013326, 181327, 12953107.
46. Schein A, Sheffy-Leven S, Glaser F, Schuster G. The RNase E/G-type endoribonuclease of higher plants is located in the chloroplast and cleaves RNA similarly to the E. coli enzyme. RNA 2008, 2008(14):1057-1068.
47. Chekanova JA, Dutko JA, Mian IS, Belostotsky DA. Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3′->5′ exonuclease containing S1 and KH RNA-binding domains. Nucl Acids Res 2002, 30:695-700. 10.1093/nar/30.3.695, 100302, 11809881.
48. Worbs M, Bourenkov GP, Bartunik HD, Huber R, Wahl MC. An extended RNA binding surface through arrayed S1 and KH domains in transcription factor NusA. Mol Cell 2011, 7:1177-1189.
49. Stickney LM, Hankins JS, Miao X, Mackie GA. Function of the conserved S1 and KH domains in polynucleotide phosphorylase. J Bacteriol 2005, 187:7214-7221. 10.1128/JB.187.21.7214-7221.2005, 1272994, 16237005.
50. Eklund EA, Lee S, Skalnik DG. Cloning of a cDNA encoding a human DNA-binding protein similar to ribosomal protein S1. Gene 1995, 155:231-235. 10.1016/0378-1119(94)00898-3, 7721096.
51. Majeran W, Friso G, Asakura Y, Qu X, Huang M, Ponnala L, Watkins KP, Barkan A, van Wijk KJ. Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol 2012, 158:156-189. 10.1104/pp.111.188474, 3252073, 22065420.
52. Romanowska E, Drożak A. Comparative analysis of biochemical properties of mesophyll and bundle sheath chloroplasts from various subtypes of C4 plants grown at moderate irradiance. Acta Bioch Pol 2006, 53:709-719.
53. Simcox PD, Garland W, Deluca V, Canvin DT, Dennis DT. Respiratory pathways and fat synthesis in the developing castor-oil seed. Can J Bot 1979, 57:1008-1014.
54. Ruuska SA, Girke T, Benning C, Ohlrogge JB. Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 2002, 14:1191-1206. 10.1105/tpc.000877, 150774, 12084821.
55. Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y. Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 2004, 432:779-782. 10.1038/nature03145, 15592419.
56. Berry JO, Nikolau BJ, Carr JP, Klessig DF. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol 1985, 5:2238-2246. 366949, 3837189.
57. Yamamoto N, Mukai Y, Matsuoka M, Kano-Murakami Y, Tanaka Y, Oshashi Y, Ozeki Y, Odani K. Light-independent expression of cab and rbcS genes in dark-grown pine seedlings. Plant Physiol 1991, 95:379-383. 10.1104/pp.95.2.379, 1077541, 16667994.
58. Maeda Y, Minamikawa T, Xu B-M. Metabolic activities in germinated ancient lotus seeds. J Exp Bot 1996, 47:577-582.
59. Romanowska E, Kargul J, Powikrowska M, Finazzi G, Nield J, Drozak A, Pokorska B. Structural organization of photosynthetic apparatus in agranal chloroplasts of maize. J Biol Chem 2008, 283:26037-26046. 10.1074/jbc.M803711200, 3258860, 18632664.
60. Kleine T, Maier UG, Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 2009, 60:115-138. 10.1146/annurev.arplant.043008.092119, 19014347.
61. Zhelyazkova P, Sharma CM, Förstner KU, Liere K, Vogel J, Börner T. The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 2012, 2012(24):123-136.
62. Mullet JE, Klein RR. Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMB0 J 1987, 6:1571-1579.
63. Whitney SM, Andrews TJ. The gene for the ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) small subunit relocated to the plastid genome of tobacco directs the synthesis of small subunits that assemble into Rubisco. Plant Cell 2001, 13:193-205. 102209, 11158539.
64. Chalker-Scott L. Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 1999, 70:1-9.
65. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 2006, 140:637-646. 10.1104/pp.105.072579, 1361330, 16384906.
66. Long JJ, Berry JO. Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. Plant Physiol 1996, 112:473-482. 157970, 12226404.
67. Bowman SM, Drzewiecki KD, Mojica E-R, Zielinski AM, Siegel A, Aga DA, Berry JO. Toxicity and reductions in intracellular calcium levels following?uptake of a tetracycline antibiotic in Arabidopsis. Environ Sci&Technol 2011, 45:8958-8964. 10.1021/es200863j, 24058731.
68. Rodermel SR, Abbott MS, Bogorad L. Nuclear-organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 1988, 55:673-681. 10.1016/0092-8674(88)90226-7, 3052855.
69. Whitney SM, von Caemmerer S, Hudson GS, Andrews TJ. Directed mutation of the rubisco large subunit of tobacco influences photorespiration and growth. Plant Physiol 1999, 121:579-588. 10.1104/pp.121.2.579, 59421, 10517850.
70. Dhingra A, Portis AR, Daniell H. Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. Proc Natl Acad Sci U S A 2004, 101:6315-6320. 10.1073/pnas.0400981101, 395966, 15067115.
71. Ichikawa K, Miyake C, Iwano M, Sekine M, Shinmyo A, Kato K. Ribulose 1,5-bisphosphate carboxylase/oxygenase large subunit translation is regulated in a small subunit-independent manner in the expanded leaves of tobacco. Plant Cell Physiol 2008, 49:214-225.
72. Feiz L, Williams-Carrier R, Wostrikoff K, Belcher S, Barkan A, Stern DB. Ribulose-1,5-bis-phosphate carboxylase/oxygenase accumulation factor1 is required for holoenzyme assembly in maize. Plant Cell 2012, 24:3435-3466. 10.1105/tpc.112.102012, 3462642, 22942379.
73. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 2012, 63:1637-1661. 10.1093/jxb/ers013, 22371324.
74. Barnes D, Mayfield SP. Redox control of posttranscriptional processes in the chloroplast. Antiox Redox Sig 2003, 5:89-94.
75. Raghavendra AS. Padmasre: beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 2003, 8:546-553. 10.1016/j.tplants.2003.09.015, 14607100.
76. Puthiyaveetil S, Ibrahim IM, Allen JF. Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts. Plant Cell Environ 2012, 35:347-359. 10.1111/j.1365-3040.2011.02349.x, 21554328.
77. Rossel JB, Wilson IW, Pogson BJ. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 2002, 130:1109-1120. 10.1104/pp.005595, 166632, 12427978.
78. Liu M-J, Wu S-H, Chen H-M, Wu S-H. Widespread translational control contributes to the regulation of Arabidopsis photomorphogenesis. Mol Sys Biol 2012, 8:566.
79. Park SH, Chung PJ, Juntawong P, Bailey-Serres J, Kim YS, Jung H, Bang SW, Kim YK, Do Choi Y, Kim JK. Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice. Plant Physiol 2012, 159:1111-1124. 10.1104/pp.112.194928, 3387698, 22566494.
80. Paul MJ, Foyer CH. Sink regulation of photosynthesis. J Exp Bot 2001, 52:1383-1400. 10.1093/jexbot/52.360.1383, 11457898.
81. Maier A, Zell MB, Maurino VG. Malate decarboxylases: evolution and roles of NAD(P)-ME isoforms in species performing C4 and C3 photosynthesis. J Exp Bot 2010, 62:3061-3069.
82. Weissmann S, Brutnell TP. Engineering C4 photosynthetic regulatory networks. Curr Opin Biotechnol 2012, 23:298-304. 10.1016/j.copbio.2011.12.018, 22261559.
83. Lee KP, Kim C, Landgraf F, Apel K. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci U S A 2007, 104:10270-10275. 10.1073/pnas.0702061104, 1891253, 17540731.
84. Slesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z. The role of hydrogen peroxide in regulation of plant metabolism and cellular signaling in response to environmental stresses. Acta Biochim Pol 2007, 54:39-50.
85. Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM. Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genom 2006, 25:142-152.
86. Acevedo-Hernandez GJ, Leon P, Herrera-Estrella LR. Sugar and ABA responsiveness of a minimal RBCS light-responsive unit is mediated by direct binding of ABI4. Plant J 2005, 43:506-519. 10.1111/j.1365-313X.2005.02468.x, 16098105.
87. Langdale JA, Kidner CA. Bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves. Development 1994, 120:673-681.
88. May BP, Martienssen RA. Transposon mutagenesis in the study of plant development. Crit Rev Plant Sci 2003, 22:1-35.
89. Lisch D. Mutator transposons. Trends Plant Sci 2002, 11:498-504.
90. Barkan A, Martienssen RA. Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. Proc Natl Acad Sci U S A 1991, 88:3502-3506. 10.1073/pnas.88.8.3502, 51476, 1849660.
91. Ortiz DF, Strommer JN. The Mu1 maize transposable element induces tissue-specific aberrant splicing and polyadenylation in two Adh1 mutants. Mol Cell Biol 1990, 10:2090-2095. 360556, 2157968.
92. Hudson GS, Mahon JD, Anderson PA, Gibbs MJ, Badger MR, Andrews T, Whitfeld PR. Comparisons of rbcL genes for the large subunit of ribulose-bisphosphate carboxylase from closely related C3 and C4 plant species. J Biol Chem 1990, 265:808-814.
93. Patel M, Corey AC, Yin L-Y, Ali S, Taylor WC, Berry JO. Untranslated regions from C4 amaranth AhRbcS1 mRNAs confer translational enhancement and preferential bundle sheath cell expression in transgenic C4Flaveria bidentis. Plant Physiol 2004, 136:3550-3561. 10.1104/pp.104.051508, 527154, 15489276.
94. Wang J-L, Klessig DF, Berry JO. Regulation of C4 gene expression in developing amaranth leaves. Plant Cell 1992, 4:173-184. 160118, 12297645.
95. McCormac DJ, Boinski JJ, Ramsperger VC, Berry JO. C4 Gene expression in photosynthetic and non-photosynthetic leaf regions of Amaranthus tricolor. Plant Physiol 1997, 114:801-815. 158366, 12223743.
96. Wesley SV, Helliwell CA, Smith NA, Wang NB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM. Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 2001, 27:581-590. 10.1046/j.1365-313X.2001.01105.x, 11576441.
97. Bent A. Arabidopsis thaliana floral dip transformation method. Methods Mol Biol 2006, 343:87-103.
98. Barkan A. Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Meth Enzymol 1998, 297:38-57.
99. Barkan A. Genome-wide analysis of RNA-protein interactions in plants. Meth Mol Biol 2009, 553:13-37.