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Euchromatin and Pericentromeric Heterochromatin: Comparative Composition in the Tomato Genome

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Euchromatin and Pericentromeric Heterochromatin: Comparative Composition in the Tomato Genome Copyright Ó 2006 by the Genetics Society of America DOI: 10.1534/genetics.106.055772 Euchromatin and Pericentromeric Heterochromatin: Comparative Composition in the Tomato Genome Ying Wang,*,†,1 Xiaomin Tang,‡ Zhukuan Cheng,‡ Lukas Mueller,*,† Jim Giovannoni§,** and Steve D. Tanksley*,†,2 *Department of Plant Breeding and Genetics, †Department of Plant Biology, §Boyce Thompson Institute for Plant Research and **U.S. Department of Agriculture–Agricultural Research Service, Plant, Soil, and Nutrition Lab, Cornell University, Ithaca, New York 14853 and ‡Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, People’s Republic of China Manuscript received October 18, 2005 Accepted for publication February 6, 2006 ABSTRACT Eleven sequenced BACs were annotated and localized via FISH to tomato pachytene chromosomes providing the first global insights into the compositional differences of euchromatin and pericentromeric heterochromatin in this model dicot species. The results indicate that tomato euchromatin has a gene density (6.7 kb/gene) similar to that of Arabidopsis and rice. Thus, while the euchromatin comprises only 25% of the tomato nuclear DNA, it is sufficient to account for 90% of the estimated 38,000 non- transposon genes that compose the tomato genome. Moreover, euchromatic BACs were largely devoid of transposons or other repetitive elements. In contrast, BACs assigned to the pericentromeric hetero- chromatin had a gene density 10–100 times lower than that of the euchromatin and are heavily populated by retrotransposons preferential to the heterochromatin—the most abundant transposons belonging to the Jinling Ty3/gypsy-like retrotransposon family. Jinling elements are highly methylated and rarely transcribed. Nonetheless, they have spread throughout the pericentromeric heterochromatin in tomato and wild tomato species fairly recently—well after tomato diverged from potato and other related sola- naceous species. The implications of these findings on evolution and on sequencing the genomes of tomato and other solanaceous species are discussed. ANY plant and animal species possess chromo- well as the structure and function of the heterochro- M somes differentiated into highly condensed, matin. The Ty3/Gypsy class retrotransposons and their pericentromeric heterochromatin and largely decon- relatives have been found in pericentromeric regions, densed euchromatic arms. In animals, heterochroma- especially in grasses (Cheng et al. 2002; Jiang et al. 2003; tin is often associated with transcriptional inactivity and Mroczek and Dawe 2003; Wu et al. 2004). Tandem suppressed genetic recombination and contains a large repeats and retroelements are also keys for centromere number of repetitive sequences (Dean and Schmidt recognition by kinetochore proteins. Repeats in the 1995; Renauld and Gasser 1997; Myster et al. 2004). pericentromeric regions also play important roles in In plants, more is known about the gene-rich euchro- sufficiently initiating the recruitment of histone modi- matin, but less about heterochromatin (De Jong 1998; fication enzymes and promoting the formation and Cheng and Murata 2003; Koornneef et al. 2003). maintenance of heterochromatin by RNAi machinery Studies thus far suggest that plant heterochromatin, (Cheng et al. 2002; Hall et al. 2002; Volpe et al. 2002; while gene poor compared with euchromatin, still con- Zhong et al. 2002; Bender 2004; Sun et al. 2004). This tains transcriptionally active genes, at least at certain still leaves open several important questions: What are times during the life cycle (Martin et al. 1993; Li et al. the global differences between euchromatin and het- 2004; Lippman et al. 2004; Martienssen et al. 2004; erochromatin? Which of these differences are consis- Nagaki et al. 2004). tent among species and which are species specific? What Advances in the genomic sequencing of model plants evolutionary forces have molded the composition and and animals have provided great insight into the com- function of heterochromatin vs. euchromatin? In hopes position and organization of genes in euchromatin as of shedding light on these questions, we have conducted a series of molecular cytogenetic experiments to char- acterize the nature of heterochromatin vs. euchromatin 1Present address: Wuhan Botanical Garden, Chinese Academy of in the model crop plant—tomato. Science, Wuhan, Hubei, People’s Republic of China, 430074. The tomato (Solanum lycopersicum) is a diploid species 2Corresponding author: Department of Plant Breeding and Genetics, 248 Emerson Hall, Cornell University, Ithaca, NY 14853. with a genome composed of 12 chromosomes (2n ¼ E-mail: [email protected] 2x ¼ 24) totaling 950 Mb of DNA (Arumuganathan et al. Genetics 172: 2529–2540 (April 2006) 2530 Y. Wang et al. 1991). Along with maize, it was an early model system repetitive elements in two ways. First, each was compared for genetics and cytogenetics studies in plants (for re- against two repeat databases: Solanaceae repeat database, view, see Rick 1971). Like many other plant species, such which contains all known repeats from solanaceous species, and Repbase, which is a comprehensive database of repetitive as Arabidopsis and Medicago truncatula, tomato chromo- element consensus sequences in eukaryotic genomes, includ- somes contain long, contiguous stretches of euchromatin ing transposable elements (TEs) and tandem repeats of at the distal ends of most chromosomes and hetero- diverse origins ( Jurka 2000; Ouyang and Buell 2004). If chromatic regions flanking the centromeres (De Jong the gene model was homologous with known TEs (TIGR_ 1998; Kulikova et al. 2001; Fransz et al. 2003). Ap- Sol_repeat, or Repbase repeats, or Arabidopsis TEs), then it was annotated as a TE-related gene. Second, the BACs were proximately 25% of the tomato genome is contained in computationally screened against each other (blastn; E-value the euchromatin and 75% is contained in the pericen- ,10ÿ20 and bits score .100) in an effort to identify repetitive tromeric heterochromatin (Peterson et al. 1998). Al- sequence motifs shared by two or more BACs. Segments of though much work has been done on Arabidopsis, which BACs containing putative repetitive elements were aligned has relatively little heterochromatin, tomato would be and manually examined in an effort to determine the length and boundaries of each repetitive element. more similar to the majority of plants, with less known Southern hybridization: A subset of the repetitive elements on the global organization of euchromatin and hetero- identified in this study was screened against the genomes of chromatin, especially crop plants that have large ge- other solanaceous species to determine the taxonomic distri- nomes and more heterochromatin. We report herein bution of these elements. For these studies, PCR-amplified 32 the annotation of 11 sequenced BAC clones assigned, repeats were amplified, labeled with P, and used as probes on the genomic Southern blots containing restriction-digested via in situ hybridization, to both euchromatin and het- genomic DNA from S. pimpinellifolium L. (LA1589), S. chmie- erochromatin. From a comparative analysis of these BACs lewskii (C. M. Rick, E. Kesicki, J. Fobes, M. Holle, D. M. Spooner, emerges a general picture of the global organization G. J. Anderson, and R. K. Jansen) (LA1316), S. peruvianum L. and evolution of euchromatin vs. heterochromatin in (LA1708), S. chilense (Dunal) Reiche (LA1959), S. pennellii this model dicot plant species. Correll (TA56), S. neorickii (D. M. Spooner, G. J. Anderson, and R. K. Jansen) (LA2133), S. habrochaites (S. Knapp and D. M. Spooner) (LA1777), S . lycopersicum L. (TA209), S. tuberosum L., MATERIALS AND METHODS Capsicum annuum L. (garden pepper), Petunia 3 hybrida hort. ex E. Vilm., and S. melongena L. (eggplant) (Spooner et al. 2005). BAC clones and annotation: Eleven sequenced tomato Blots were hybridized at 60° and washed in 23 SSC for 20 min nuclear BAC clones were included in the analyses described and in 13 SSC for 10 min. The tomato 45S rDNA (R45S) herein. The sequences of all BACs have been submitted to ribosomal gene probe was used as a positive control for GenBank (see Table 1 for accession numbers). Three BACs estimating the relative strength of hybridization signals (181K1, 181O9, and 181C9) were randomly selected from a (Ganal et al. 1988). tomato BAC library, whereas the other 8 were isolated from the For estimating the methylation status of cytosine in the same library by virtue of screening with known genes or single- retrotransposons, a Southern blot was made using tomato copy probes (Budiman et al. 2000; van der Hoeven et al. 2002; (TA56 and TA209) genomic DNA digested with methylation- Y. Wang, unpublished data). All BACs were subjected to sensitive restriction enzymes, HpaII and EcoRI, and methyla- annotation according to guidelines utilized for the rice and tion insensitive isoschizomers, MspI and BstNI (Messeguer Arabidopsis genome (Mao et al. 2001; Goff et al. 2002; Yuet al. et al. 1991). The LTR and polyprotein regions of the retro- 2002; International Rice Genome Sequencing Project transposon were labeled with 32P-dCTP and used as probes on 2005). Genes were predicted with four computational gene- the genomic Southern blots. Since cytosines in the tomato finder programs: FGENESH (Salamov and Solovyev 2000), chloroplast are not methylated, PCR fragments of tomato GenemarkHMM (Borodovsky and McIninch 1993), Genscan1 chloroplast genes (AY216521, AF397080, and AF263101)
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