Rapid divergence and expansion of the papaya X

Rapid divergence and expansion of the papaya X chromosome compared to its ancestral autosome Andrea R. Gschwend 1, Qingyi Yu 2, Fanchang Zeng 1, Robert Van. Buren 1, Rishi Aryal 1, Jennifer Han 1, Ray Ming 1 1. 2. Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA Texas Agri. Life Research, Texas A&M University, Weslaco, Texas 78596, USA Introduction: It has long been thought that, while the hemizygous Y chromosome changes drastically over time, the X chromosome conserves the ancestral autosome content and structure. To determine whether the X chromosome remains unchanged compared to its ancestral autosome, BAC sequences of Carica papaya and Vasconcellea monoica were analyzed. Carica papaya is a trioecious tropical plant with very young sex chromosomes (2 -3 my), the segregation of which results in male (XY), female (XX), and hermaphrodite (XYh) individuals. Close relative Vasconcellea monoica, which diverged from a shared common ancestor with papaya 6. 8 -14. 7 mya, is monoecious, having separate male and female flowers on a single individual, with the lack of sexual dimorphism, signifying the absence of sex chromosomes. The genome size of monoica is 626 Mb compared to the 372 Mb genome of papaya, signifying expansion in monoica since the divergence of these species. The retention of the ancestral autosome in monoica and difference in sexual systems between closely related papaya and monoica allow for a unique opportunity to better understand early X chromosome evolution. Results: Table 1. Summary of the repetitive element content of the papaya and monoica BACs. The papaya X-specific region, overall, expanded 48%, where as the monoica autosome expanded 62%. The autosomal expansion in monoica is consistent with the larger monoica genome size and is largely due to an increase of repetitive elements across the autosome. The expansion of the papaya X-specific region is due to the lack of recombination between the HSY and X regions of the sex chromosomes, which, over time, allowed for the accelerated accumulation of repetitive elements. The suppression of recombination also allowed for the accumulation of autosomal genes and gene shuffling in the papaya sex specific region. Though the X-specific region evolves slower then the Yspecific region, it is not as static as previously thought. a) papaya Xspecific BACs monoica corresponding BACs b) papaya autosomal BAC monoica corresponding BAC 45% Retroelements LINEs LTR elements DNA transposons Unclassified Total interspersed repeats 56% 101. 3 kb 2. 56 Mb Figure 1. a) Expansion in the syntenic regions of 16 BACs and 2 contigs found in the papaya X-specific region compared to its corresponding 11 monoica BACs. b) Expansion of the syntenic region of one monoica autosomal BAC compared to its corresponding papaya autosomal BAC. 60. 2% Table 2. Gene density of the papaya and monoica BACs monoica Papaya X Sequence Gene Density length (in kb) (per 100 Kb) 703 2. 84 1, 821 2. 58 monoica 99 7. 14 papaya autosome 58 10. 34 Conclusions: 5% 1. 1 Mb 65. 4% Papaya X-specific BACS (2, 545 kb) 62% 72. 8 kb 46. 4% 0. 9% 45. 6% 0. 1% 18. 9% monoica X region BACS (1, 082 kb) 32. 5% 1. 4% 31. 1% 26. 5% papaya genome monoica autosome (271, 000 kb) BAC (102 kb) 42. 2% 1. 1% 41. 1% 0. 2% 8. 7% 28. 4% 7. 8% 20. 6% 0. 7% 31. 4% 51. 2% 60. 5% Table 3. Gene content of the papaya and monoica BACs Total transcription units-SDR Total pseudogenes-SDR Paired Vm-X-HSY paired Vm-X or Vm-HSY Vm-Specific X-Specific Total transcription units-Autosome Paired Vm-Specific X-Specific Total Genes Vm Cp X/A 20 47 5 9 33 10 23 0 10 13 7 6 6 1 0 *SDR-Sex determining region, HSY-hermaphrodite specific region of the Y chromosome v The papaya X-specific region showed marked expansion compared to the ancestral autosome in monoica. The monoica autosome expanded compared to the corresponding autosomal BAC in papaya, consistent with genome size differences. v The expansion of the papaya X-specific region is largely due to the increase of repetitive elements, specifically LTR retrotransposons. v The papaya sex specific regions gained a considerable number of genes compared to the corresponding monoica region. The autosomal region of papaya and monoica, had a greater gene density and the majority of genes and gene order were conserved between the two species. Acknowledgments: This research was funded by the NSF Plant Genome Research Program (award number 0553417).