Transcriptional Activity, Chromosomal Distribution and Expression Effects of Transposable Elements in Coffea Genomes

Plant genomes are massively invaded by transposable elements (TEs), many of which are located near host genes and can thus impact gene expression. In flowering plants, TE expression can be activated (de-repressed) under certain stressful conditions, both biotic and abiotic, as well as by genome stress caused by hybridization. In this study, we examined the effects of these stress agents on TE expression in two diploid species of coffee, Coffea canephora and C. eugenioides, and their allotetraploid hybrid C. arabica. We also explored the relationship of TE repression mechanisms to host gene regulation via the effects of exonized TE sequences. Similar to what has been seen for other plants, overall TE expression levels are low in Coffea plant cultivars, consistent with the existence of effective TE repression mechanisms. TE expression patterns are highly dynamic across the species and conditions assayed here are unrelated to their classification at the level of TE class or family. In contrast to previous results, cell culture conditions per se do not lead to the de-repression of TE expression in C. arabica. Results obtained here indicate that differing plant drought stress levels relate strongly to TE repression mechanisms. TEs tend to be expressed at significantly higher levels in non-irrigated samples for the drought tolerant cultivars but in drought sensitive cultivars the opposite pattern was shown with irrigated samples showing significantly higher TE expression. Thus, TE genome repression mechanisms may be finely tuned to the ideal growth and/or regulatory conditions of the specific plant cultivars in which they are active. Analysis of TE expression levels in cell culture conditions underscored the importance of nonsense-mediated mRNA decay (NMD) pathways in the repression of Coffea TEs. These same NMD mechanisms can also regulate plant host gene expression via the repression of genes that bear exonized TE sequences.

[1]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[2]  Daniela Kajihara,et al.  Transcriptionally active transposable elements in recent hybrid sugarcane. , 2005, The Plant journal : for cell and molecular biology.

[3]  M. Morgante,et al.  Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. , 2001, Genome research.

[4]  C. Vicient.  Transcriptional activity of transposable elements in maize , 2010, BMC Genomics.

[5]  Eric K. Tokuda,et al.  An EST-based analysis identifies new genes and reveals distinctive gene expression features of Coffea arabica and Coffea canephora , 2011, BMC Plant Biology.

[6]  C. Camilleri,et al.  Tnt1 transposition events are induced by in vitro transformation of Arabidopsis thaliana, and transposed copies integrate into genes , 2001, Molecular Genetics and Genomics.

[7]  G. Glazko,et al.  Origin of a substantial fraction of human regulatory sequences from transposable elements. , 2003, Trends in genetics : TIG.

[8]  Jean YH Yang,et al.  Bioconductor: open software development for computational biology and bioinformatics , 2004, Genome Biology.

[9]  M. Feldman,et al.  Genome Evolution Due to Allopolyploidization in Wheat , 2012, Genetics.

[10]  V. Poncet,et al.  Two novel Ty1-copia retrotransposons isolated from coffee trees can effectively reveal evolutionary relationships in the Coffea genus (Rubiaceae) , 2011, Molecular Genetics and Genomics.

[11]  H Okamoto,et al.  Silencing of transposable elements in plants. , 2001, Trends in plant science.

[12]  J. Robert,et al.  Molecular characterisation and origin of the Coffea arabica L. genome , 1999, Molecular and General Genetics MGG.

[13]  Eduardo P. Costa,et al.  Identification and frequency of transposable elements in Eucalyptus , 2005 .

[14]  D. Voytas,et al.  Rapid flux in plant genomes , 1998, Nature Genetics.

[15]  C. Biémont.  Are transposable elements simply silenced or are they under house arrest? , 2009, Trends in genetics : TIG.

[16]  T. B. dos Santos,et al.  FISH using a gag-like fragment probe reveals a common Ty3-gypsy-like retrotransposon in genome of Coffea species. , 2012, Genome.

[17]  M. Grandbastien,et al.  Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. , 2001, Plant physiology.

[18]  S. Tanksley,et al.  Coffee and tomato share common gene repertoires as revealed by deep sequencing of seed and cherry transcripts , 2005, Theoretical and Applied Genetics.

[19]  M. Caboche,et al.  Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. , 1991, The EMBO journal.

[20]  Robert A. Martienssen,et al.  Noncoding RNAs and Gene Silencing , 2007, Cell.

[21]  M. Feldman,et al.  Allopolyploidy – a shaping force in the evolution of wheat genomes , 2005, Cytogenetic and Genome Research.

[22]  M. Grandbastien.  Activation of plant retrotransposons under stress conditions , 1998 .

[23]  D. Pot,et al.  Genetics of coffee quality , 2006 .

[24]  Saverio Brogna,et al.  Nonsense-mediated mRNA decay (NMD) mechanisms , 2009, Nature Structural &Molecular Biology.

[25]  A. Levy,et al.  Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat , 2003, Nature Genetics.

[26]  N. Fedoroff,et al.  Transposons and genome evolution in plants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Doerge,et al.  Genomic changes in synthetic Arabidopsis polyploids. , 2004, The Plant journal : for cell and molecular biology.

[28]  V. Poncet,et al.  Site-Specific Insertion Polymorphism of the MITE Alex-1 in the Genus Coffea Suggests Interspecific Gene Flow , 2011, International journal of evolutionary biology.

[29]  Valer Gotea,et al.  Transposable elements as a significant source of transcription regulating signals. , 2006, Gene.

[30]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[31]  M. G. Kidwell,et al.  Transposable elements as sources of variation in animals and plants. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Bennetzen,et al.  Plant retrotransposons. , 1999, Annual review of genetics.

[33]  P. Lashermes,et al.  Genomics of Coffee One of the World’s Largest Traded Commodities , 2008 .

[34]  H. Hirochika.  Activation of tobacco retrotransposons during tissue culture. , 1993, The EMBO journal.

[35]  M. Combes,et al.  Genome evolution in diploid and tetraploid Coffea species as revealed by comparative analysis of orthologous genome segments , 2011, Plant Molecular Biology.

[36]  T. Peterson,et al.  Genome rearrangements by nonlinear transposons in maize. , 1999, Genetics.

[37]  Francisco Martinez-Murillo,et al.  Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise , 2004, Nature Genetics.

[38]  V. Poncet,et al.  Microcollinearity in an ethylene receptor coding gene region of the Coffea canephora genome is extensively conserved with Vitis vinifera and other distant dicotyledonous sequenced genomes , 2009, BMC Plant Biology.

[39]  H. Hirochika,et al.  Retrotransposons of rice involved in mutations induced by tissue culture. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Borodovsky,et al.  Evaluating the protein coding potential of exonized transposable element sequences , 2007, Biology Direct.

[41]  M. Rossi,et al.  Survey of transposable elements in sugarcane expressed sequence tags (ESTs) , 2001 .

[42]  M. Carazzolle,et al.  Transposable elements in Coffea (Gentianales: Rubiacea) transcripts and their role in the origin of protein diversity in flowering plants , 2008, Molecular Genetics and Genomics.

[43]  J. Bennetzen,et al.  Mechanisms and rates of genome expansion and contraction in flowering plants , 2002, Genetica.

[44]  T. Kakutani,et al.  Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. , 2006, The Plant journal : for cell and molecular biology.