The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants

New Phytologist

Volumn 206, Issue 1, 2015, Pages 352-367

  Alaba, Sylwia ^a   Piszczalka, Pawel ^a   Pietrykowska, Halina ^a   Pacak, Andrzej M ^a   Sierocka, Izabela ^a   Nuc, Przemyslaw W ^a   Singh, Kashmir ^a   Plewka, Patrycja ^a   Sulkowska, Aleksandra ^a   Jarmolowski, Artur ^a   Karlowski, Wojciech M ^a   Szweykowska Kulinska, Zofia ^a  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Basal lineage; Land plants; Liverwort; MicroRNA (miRNA) genes; Microtranscriptome; MiRNA precursors; MiRNA targets; Pellia endiviifolia

Indexed keywords

EVOLUTIONARY THEORY; GENE EXPRESSION; GREEN ALGA; LIVERWORT; MOLECULAR ANALYSIS; NEW RECORD; RNA;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EMBRYOPHYTA; MARCHANTIA POLYMORPHA; MARCHANTIOPHYTA; PELLIA ENDIVIIFOLIA;

MESSENGER RNA; MICRORNA; TRANSCRIPTOME;

EMBRYOPHYTA; GENE EXPRESSION REGULATION; GENETICS; GREEN ALGA; HIGH THROUGHPUT SEQUENCING; LIVERWORT; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS;

BASE SEQUENCE; CHLOROPHYTA; EMBRYOPHYTA; GENE EXPRESSION REGULATION, PLANT; HEPATOPHYTA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84923395390     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13220     Document Type: Article

References (82)

1. Abdel-Ghany SE, Pilon M. 2008. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. The Journal of Biological Chemistry 283: 15932-15945.
2. Addo-Quaye C, Miller W, Axtell MJ. 2009a. CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25: 130-131.
3. Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ. 2009b. Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15: 2112-2121.
4. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
5. Axtell MJ, Snyder JA, Bartel DP. 2007. Common functions for diverse small RNAs of land plants. Plant Cell 19: 1750-1769.
6. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA et al. 2011. The compact Selaginella genome identifies changes in gene content associated with the evolution of vascular plants. Science 332: 960-963.
7. Bielewicz D, Dolata J, Zielezinski A, Alaba S, Szarzynska B, Szczesniak MW, Jarmolowski A, Szweykowska-Kulinska Z, Karlowski WM. 2012. mirEX: a platform for comparative exploration of plant pri-miRNA expression data. Nucleic Acids Research 40: D191-D197.
8. Bologna NG, Schapire AL, Zhai J, Chorostecki U, Boisbouvier J, Meyers BC, Palatnik JF. 2013. Multiple RNA recognition patterns during microRNA biogenesis in plants. Genome Research 23: 1675-1689.
9. Bonnet E, He Y, Billiau K, Van de Peer Y. 2010. TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26: 1566-1568.
10. Bowman JL. 2013. Walk about on the long branches of plant evolution. Current Opinion in Plant Biology 16: 70-77.
11. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190.
12. Chorostecki U, Crosa VA, Lodeyro AF, Bologna NG, Martin AP, Carrillo N, Schommer C, Palatnik JF. 2012. Identification of new microRNA-regulated genes by conserved targeting in plant species. Nucleic Acids Research 40: 8893-8904.
13. Crandall-Stotler B, Stotler RE, Long DG. 2009. Phylogeny and the classification of the Marchantiophyta. Edinburgh Journal of Botany 66: 155-198.
14. Cuperus JT, Fahlgren N, Carrington JC. 2011. Evolution and functional diversification of MIRNA genes. Plant Cell 23: 431-442.
15. Dai X, Zhao PX. 2011. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research 39: W155-W159.
16. Eddy SR. 2011. Accelerated Profile HMM Searches. PLoS Computational Biology 7: e1002195.
17. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL et al. 2007. High-throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of MIRNA genes. PLoS ONE 2: e219.
18. Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D et al. 2010. MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22: 1074-1089.
19. Fattash I, Voß B, Reski R, Hess WR, Frank W. 2007. Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biology 7: 13.
20. Leu(CAA) intergenic sequences. Gene 262: 309-315.
21. Fiedorow P, Szweykowska-Kulinska Z. 1998. Intergenic sequences of clustered tRNA genes: new type of genetic marker for phylogenetic studies, with application to the taxonomy of liverworts. Plant Molecular Biology 38: 1257-1261.
22. German MA, Luo S, Schroth G, Meyers BC, Green PJ. 2009. Construction of parallel analysis of RNA ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nature Protocols 4: 356-362.
23. German MA, Pillay M, Jeong D-H, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R et al. 2008. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nature Biotechnology 26: 941-946.
24. Griffiths-Jones S. 2004. The microRNA registry. Nucleic Acids Research 32: D109-D111.
25. Guo L, Lu Z. 2010. The fate of miRNA* strand through evolutionary analysis: implication for degradation as merely carrier strand or potential regulatory molecule? PLoS ONE 5: e11387.
26. He-Nygrén X, Juslén A, Ahonen I, Glenny D, Piippo S. 2006. Illuminating the evolutionary history of liverworts (Marchantiophyta) - towards a natural classification. Cladistics 22: 1-31.
27. Iseli C, Jongeneel CV, Bucher P. 1999. ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. In: Lengauer T, Schneider R, Bork P, Brutlag DL, Glasgow JI, Mewes HW, Zimmer R, eds. Proceedings of the International Conference on Intelligent Systems for Molecular Biology. Menlo Park, CA, USA: AAAI Press, 138-158.
28. Jia F, Rock CD. 2012. MIR846 and MIR842 comprise a cistronic MIRNA pair that is regulated by abscisic acid by alternative splicing in roots of Arabidopsis. Plant Molecular Biology 81: 447-460.
29. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. 2004. Human MicroRNA Targets. PLoS Biology 2: e363.
30. Jones-Rhoades MW, Bartel DP. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14: 787-799.
31. Karol KS, McCourt RM, Cimino MT, Delwiche CF. 2001. The closest living relatives of land plants. Science 294: 2351-2353.
32. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W. 2010. Transcriptional control of gene expression by microRNAs. Cell 140: 111-122.
33. Kim VN. 2005. MicroRNA biogenesis: coordinated cropping and dicing. Nature Reviews Molecular Cell Biology 6: 376-385.
34. Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research 42: D68-D73.
35. Kruszka K, Pacak A, Swida-Barteczka A, Nuc P, Alaba S, Wroblewska Z, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z. 2014. Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. Journal of Experimental Botany 65: 6123-6135.
36. Kruszka K, Pacak A, Swida-Barteczka A, Stefaniak AK, Kaja E, Sierocka I, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z. 2013. Developmentally regulated expression and complex processing of barley pri-microRNAs. BMC Genomics 14: 34.
37. Kurichara Y, Watanabe Y. 2004. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proceedings of the National Academy of Sciences, USA 101: 12753-12758.
38. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. 2004. MicroRNA genes are transcribed by RNA polymerase II. EMBO Journal 23: 4051-4060.
39. Lenz D, May P, Walther D. 2011. Comparative analysis of miRNAs and their targets across four plant species. BMC Research Notes 4: 483-490.
40. Li J, Wu Y, Qi Y. 2013. microRNAs in a multicellular green alga Volvox carteri. Science China Life Sciences 57: 36-45.
41. Liberato JR, Barrero RW, Shivas RG. 2005. Leaf-clearing and staining techniques for the observation of conidiophores in the Phyllactinioideae (Erysiphaceae). Australian Plant Pathology 34: 401-404.
42. Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG. 2007. Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. American Journal of Botany 94: 1756-1777.
43. Llave C, Xie Z, Kasschau KD, Carrington JC. 2002. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053-2056.
44. Mao W, Li Z, Xia X, Li Y, Yu J. 2012. A Combined approach of high-throughput sequencing and degradome analysis reveals tissue specific expression of microRNAs and their targets in cucumber. PLoS ONE 7: e33040.
45. Mateos JL, Bologna NG, Corostecki U, Palatnik JF. 2010. Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Current Biology 20: 49-54.
46. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ et al. 2008. Criteria for annotation of plant microRNAs. Plant Cell 20: 3186-3190.
47. Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC. 2007. miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447: 1126-1129.
48. Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, Sahinalp SC, Unrau PJ. 2008. Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Research 18: 571-584.
49. Nishiyama R, Yamato KT, Miura K, Sakaida M, Okada S, Kono K, Takahama M, Sone T, Takenaka M, Fukuzawa H et al. 2000. Comparison of expressed sequence tags from male and female sexual organs of Marchantia polymorpha. DNA Research 7: 165-174.
50. Nozawa M, Miura S, Nei M. 2012. Origins and evolution of microRNA genes in plant species. Genome Biology and Evolution 4: 230-239.
51. Pacak A, Fiedorow P, Dabert J, Szweykowska-Kulinska Z. 1998. RAPD technique for taxonomic studies of Pellia epiphylla-complex (Hepaticae, Metzgeriales). Genetica 104: 179-187.
52. Pant B, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR. 2009. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150: 1541-1555.
53. Park W, Li J, Song R, Messing J, Chen X. 2002. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Current Biology 12: 1484-1495.
54. Provan J, Murphy S, Maggs CA. 2004. Universal plastid primers for Chlorophyta and Rhodophyta. European Journal of Phycology 39: 43-50.
55. Qiu YL, Cho Y, Cox JC, Palmer JD. 1998. The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394: 671-674.
56. Qiu YL, Li LB, Wang B, Chen ZD, Dombrovska O, Lee J, Kent L, Li RQ, Jobson RW, Hendry TA. 2007. A non-flowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial and nuclear genes. International Journal of Plant Sciences 168: 691-708.
57. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes & Development 20: 3407-3425.
58. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP. 2002. MicroRNAs in plants. Genes & Development 16: 1616-1626.
59. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. 2002. Prediction of plant microRNA targets. Cell 110: 513-520.
60. Ritchie W, Legendre M, Gautheret D. 2007. RNA stem-loops: to be or not to be cleaved by RNase III. RNA 13: 457-462.
61. Rubinstein CV, Gerrienne P, de la Puente GS, Astini RA, Steemans P. 2010. Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytologist 188: 365-369.
62. Rubio-Somoza I, Weigel D. 2011. MicroRNA networks and developmental plasticity in plants. Trends in Plant Science 16: 258-264.
63. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG. 2014. From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evolutionary Biology 14: 23.
64. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D. 2005. Specific effects of microRNAs on the plant transcriptome. Developmental Cell 8: 517-527.
65. Shao C, Ma X, Xu X, Meng Y. 2013. Identification of the highly accumulated microRNA*s in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Gene 515: 123-127.
66. Sharma N, Bhalla PL, Singh MB. 2013. Transcriptome-wide profiling and expression analysis of transcription factor families in a liverwort, Marchantia polymorpha. BMC Genomics 14: 915.
67. Sharma N, Jung C-H, Bhalla PL, Singh MB. 2014. RNA sequencing analysis of the gametophyte transcriptome from the liverwort, Marchantia polymorpha. PLoS ONE 9: e97497.
68. Sierocka I, Rojek A, Bielewicz D, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z. 2011. Novel genes specifically expressed during the development of the male thalli and antheridia in the dioecious liverwort Pellia endiviifolia. Gene 485: 53-62.
69. Simon L, Lalonde M, Bruns TD. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Applied and Environmental Microbiology 58: 291-295.
70. Sobkowiak L, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z. 2012. Non-canonical processing of Arabidopsis pri-miR319a/b/c generates additional microRNAs to target one RAP2.12 mRNA isoform. Frontiers in Plant Sciences 3: 46.
71. Song L, Axtell MJ, Fedoroff NV. 2010. RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Current Biology 20: 37-41.
72. Sonnhammer EL, Eddy SR, Durbin R. 1997. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28: 405-420.
73. Sunkar R, Zhu JK. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019.
74. Szarzynska B, Sobkowiak L, Pant BD, Balazadeh S, Scheible WR, Mueller-Roeber B, Jarmolowski A, Szweykowska-Kulinska Z. 2009. Gene structures and processing of Arabidopsis thaliana HYL1-dependent pri-miRNAs. Nucleic Acids Research 37: 3083-3093.
75. Tang G, Reinhart BJ, Bartel DP, Zamore PD. 2003. A biochemical framework for RNA silencing in plants. Genes and Development 17: 49-63.
76. Taylor RS, Tarver JE, Hiscock SJ, Donoghue PC. 2014. Evolutionary history of plant microRNAs. Trends in Plant Science 19: 175-182.
77. Timme RE, Bachvaroff TR, Delwiche CF. 2012. Broad phylogenetic sampling and sister lineage of land plants. PLoS ONE 7: e29696.
78. Voinnet O. 2009. Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.
79. Yamato KT, Ishizaki K, Fujisawa M, Okada S, Nakayama S, Fujishita M, Bando H, Yodoya K, Hayashi K, Bando T et al. 2007. Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proceedings of the National Academy of Sciences, USA 104: 6472-6477.
80. Zhang Z, Yu J, Li D, Zhang Z, Liu F, Zhou X, Wang T, Ling Y, Su Z. 2010. PMRD: plant microRNA database. Nucleic Acids Research 38: D806-D813.
81. Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ, Qi Y. 2007. A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes and Development 21: 1190-1203.
82. Zhu H, Xia R, Zhao B, An YQ, Dardick CD, Callahan AM, Liu Z. 2012. Unique expression, processing regulation, and regulatory network of peach (Prunus persica) miRNAs. BMC Plant Biology 12: 149.