The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome

Hurst, Laurence D., Ghanbarian, Avazeh T., Forrest, Alistair R. R., Huminiecki, Lukasz, Rehli, Michael, Baillie, J. Kenneth, de Hoon, Michiel J. L., Haberle, Vanja, Lassmann, Timo, Kulakovskiy, Ivan V., Lizio, Marina, Itoh, Masayoshi, Andersson, Robin, Mungall, Christopher J., Meehan, Terrence F., Schmeier, Sebastian, Bertin, Nicolas, Jorgensen, Mette, Dimont, Emmanuel, Arner, Erik, Schmidl, Christian, Schaefer, Ulf, Medvedeva, Yulia A., Plessy, Charles, Vitezic, Morana, Severin, Jessica, Semple, Colin A., Ishizu, Yuri, Young, Robert S., Francescatto, Margherita, Alam, Intikhab, Albanese, Davide, Altschuler, Gabriel M., Arakawa, Takahiro, Archer, John A. C., Arner, Peter, Babina, Magda, Baker, Sarah, Balwierz, Piotr J., Beckhouse, Anthony G., Pradhan, Swati, Blake, Judith A., Blumenthal, Antje, Bodega, Beatrice, Bonetti, Alessandro, Briggs, James, Brombacher, Frank, Burroughs, A. Maxwell, Califano, Andrea, Cannistraci, Carlo V., Carbajo, Daniel, Chen, Yun, Chierici, Marco, Ciani, Yari, Clevers, Hans C., Dalla, Emiliano, Davis, Carrie A., Detmar, Michael, Diehl, Alexander D., Dohi, Taeko, Drablos, Finn, Edge, Albert S. B., Edinger, Matthias, Ekwall, Karl, Endoh, Mitsuhiro, Enomoto, Hideki, Fagiolini, Michela, Fairbairn, Lynsey, Fang, Hai, Farach-Carson, Mary C., Faulkner, Geoffrey J., Favorov, Alexander V., Fisher, Malcolm E., Frith, Martin C., Fujita, Rie, Fukuda, Shiro, Furlanello, Cesare, Furuno, Masaaki, Furusawa, Jun-ichi, Geijtenbeek, Teunis B., Gibson, Andrew ., Gingeras, Thomas, Goldowitz, Daniel, Gough, Julian, Guhl, Sven, Guler, Reto, Gustincich, Stefano, Ha, Thomas J., Hamaguchi, Masahide, Hara, Mitsuko, Harbers, Matthias, Harshbarger, Jayson, Hasegawa, Akira, Hasegawa, Yuki, Hashimoto, Takehiro, Herlyn, Meenhard, Hitchens, Kelly J., Ho Sui, Shannan J., Hofmann, Oliver M., Hoof, Ilka, Hori, Fumi, Huminiecki, Lukasz, Iida, Kei, Ikawa, Tomokatsu, Jankovic, Boris R., Jia, Hui, Joshi, Anagha, Jurman, Giuseppe, Kaczkowski, Bogumil, Kai, Chieko, Kaida, Kaoru, Kaiho, Ai, Kajiyama, Kazuhiro, Kanamori-Katayama, Mutsumi, Kasianov, Artem S., Kasukawa, Takeya, Katayama, Shintaro, Kato, Sachi, Kawaguchi, Shuji, Kawamoto, Hiroshi, Kawamura, Yuki I., Kawashima, Tsugumi, Kempfle, Judith S., Kenna, Tony J., Kere, Juha, Khachigian, Levon M., Kitamura, Toshio, Klinken, S. Peter, Knox, Alan J., Kojima, Miki, Kojima, Soichi, Kondo, Naoto, Koseki, Haruhiko, Koyasu, Shigeo, Krampitz, Sarah, Kubosaki, Atsutaka, Kwon, Andrew T., Laros, Jeroen F. J., Lee, Weonju, Lennartsson, Andreas, Li, Kang, Lilje, Berit, Lipovich, Leonard, Mackay, Alan, Manabe, Riichiroh, Mar, Jessica C., Marchand, Benoit, Mathelier, Anthony, Mejhert, Niklas, Meynert, Alison, Mizuno, Yosuke, de Lima Morais, David A., Morikawa, Hiromasa, Morimoto, Mitsuru., Moro, Kazuyo, Motakis, Efthymios, Motohashi, Hozumi, Mummery, Christine L., Murata, Mitsuyoshi, Nagao-Sato, Sayaka, Nakachi, Yutaka, Nakahara, Fumio, Nakamura, Toshiyuki, Nakamura, Yukio, Nakazato, Kenichi, van Nimwegen, Erik, Ninomiya, Noriko, Nishiyori, Hiromi, Noma, Shohei, Nozaki, Tadasuke, Ogishima, Soichi, Ohkura, Naganari, Ohmiya, Hiroko, Ohno, Hiroshi, Ohshima, Mitsuhiro, Okada-Hatakeyama, Mariko, Okazaki, Yasushi, Orlando, Valerio, Ovchinnikov, Dmitry A., Pain, Arnab, Passier, Robert, Patrikakis, Margaret, Persson, Helena, Piazza, Silvano, Prendergast, James G. D., Rackham, Owen J. ., Ramilowski, Jordan A., Rashid, Mamoon, Ravasi, Timothy, Rizzu, Patrizia, Roncador, Marco, Roy, Sugata, Rye, Morten B., Saijyo, Eri, Sajantila, Antti, Saka, Akiko, Sakaguchi, Shimon, Sakai, Mizuho, Sato, Hiroki, Satoh, Hironori, Savvi, Suzana, Saxena, Alka, Schneider, Claudio, Schultes, Erik A., Schulze-Tanzil, Gundula G., Schwegmann, Anita, Sengstag, Thierry, Sheng, Guojun, Shimoji, Hisashi, Shimoni, Yishai, Shin, Jay W., Simon, Christophe, Sugiyama, Daisuke, Sugiyama, Takaaki, Suzuki, Masanori, Suzuki, Naoko, Swoboda, Rolf K., 't Hoen, Peter A.C., Tagami, Michihira, Takahashi, Naoko, Takai, Jun, Tanaka, Hiroshi, Tatsukawa, Hideki, Tatum, Zuotian, Thompson, Mark, Toyoda, Hiroo, Toyoda, Tetsuro, Valen, Eivind, van de Wetering, Marc, van den Berg, Linda M., Verardo, Roberto, Vijayan, Dipti, Vorontsov, Ilya E., Wasserman, Wyeth W., Watanabe, Shoko, Wells, Christine A., Winteringham, Louise N., Wolvetang, Ernst, Wood, Emily J., Yamaguchi, Yoko, Yamamoto, Masayuki, Yoneda, Misako, Yonekura, Yohei, Yoshida, Shigehiro, Zabierowski, Suzan E., Zhang, Peter G., Zhao, Xiaobei, Zucchelli, Silvia, Summers, Kim M., Suzuki, Harukazu, Daub, Carsten O., Kawai, Jun, Heutink, Peter, Hide, Winston, Freeman, Tom C., Lenhard, Boris, Bajic, Vladimir B., Taylor, Martin S., Makeev, Vsevolod J., Sandelin, Albin, Hume, David A., Carninci, Piero and Hayashizaki, Yoshihide (2015) The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome. PLoS Biology, 13 12: . doi:10.1371/journal.pbio.1002315


Author Hurst, Laurence D.
Ghanbarian, Avazeh T.
Forrest, Alistair R. R.
Huminiecki, Lukasz
Rehli, Michael
Baillie, J. Kenneth
de Hoon, Michiel J. L.
Haberle, Vanja
Lassmann, Timo
Kulakovskiy, Ivan V.
Lizio, Marina
Itoh, Masayoshi
Andersson, Robin
Mungall, Christopher J.
Meehan, Terrence F.
Schmeier, Sebastian
Bertin, Nicolas
Jorgensen, Mette
Dimont, Emmanuel
Arner, Erik
Schmidl, Christian
Schaefer, Ulf
Medvedeva, Yulia A.
Plessy, Charles
Vitezic, Morana
Severin, Jessica
Semple, Colin A.
Ishizu, Yuri
Young, Robert S.
Francescatto, Margherita
Alam, Intikhab
Albanese, Davide
Altschuler, Gabriel M.
Arakawa, Takahiro
Archer, John A. C.
Arner, Peter
Babina, Magda
Baker, Sarah
Balwierz, Piotr J.
Beckhouse, Anthony G.
Pradhan, Swati
Blake, Judith A.
Blumenthal, Antje
Bodega, Beatrice
Bonetti, Alessandro
Briggs, James
Brombacher, Frank
Burroughs, A. Maxwell
Califano, Andrea
Cannistraci, Carlo V.
Carbajo, Daniel
Chen, Yun
Chierici, Marco
Ciani, Yari
Clevers, Hans C.
Dalla, Emiliano
Davis, Carrie A.
Detmar, Michael
Diehl, Alexander D.
Dohi, Taeko
Drablos, Finn
Edge, Albert S. B.
Edinger, Matthias
Ekwall, Karl
Endoh, Mitsuhiro
Enomoto, Hideki
Fagiolini, Michela
Fairbairn, Lynsey
Fang, Hai
Farach-Carson, Mary C.
Faulkner, Geoffrey J.
Favorov, Alexander V.
Fisher, Malcolm E.
Frith, Martin C.
Fujita, Rie
Fukuda, Shiro
Furlanello, Cesare
Furuno, Masaaki
Furusawa, Jun-ichi
Geijtenbeek, Teunis B.
Gibson, Andrew .
Gingeras, Thomas
Goldowitz, Daniel
Gough, Julian
Guhl, Sven
Guler, Reto
Gustincich, Stefano
Ha, Thomas J.
Hamaguchi, Masahide
Hara, Mitsuko
Harbers, Matthias
Harshbarger, Jayson
Hasegawa, Akira
Hasegawa, Yuki
Hashimoto, Takehiro
Herlyn, Meenhard
Hitchens, Kelly J.
Ho Sui, Shannan J.
Hofmann, Oliver M.
Hoof, Ilka
Hori, Fumi
Huminiecki, Lukasz
Iida, Kei
Ikawa, Tomokatsu
Jankovic, Boris R.
Jia, Hui
Joshi, Anagha
Jurman, Giuseppe
Kaczkowski, Bogumil
Kai, Chieko
Kaida, Kaoru
Kaiho, Ai
Kajiyama, Kazuhiro
Kanamori-Katayama, Mutsumi
Kasianov, Artem S.
Kasukawa, Takeya
Katayama, Shintaro
Kato, Sachi
Kawaguchi, Shuji
Kawamoto, Hiroshi
Kawamura, Yuki I.
Kawashima, Tsugumi
Kempfle, Judith S.
Kenna, Tony J.
Kere, Juha
Khachigian, Levon M.
Kitamura, Toshio
Klinken, S. Peter
Knox, Alan J.
Kojima, Miki
Kojima, Soichi
Kondo, Naoto
Koseki, Haruhiko
Koyasu, Shigeo
Krampitz, Sarah
Kubosaki, Atsutaka
Kwon, Andrew T.
Laros, Jeroen F. J.
Lee, Weonju
Lennartsson, Andreas
Li, Kang
Lilje, Berit
Lipovich, Leonard
Mackay, Alan
Manabe, Riichiroh
Mar, Jessica C.
Marchand, Benoit
Mathelier, Anthony
Mejhert, Niklas
Meynert, Alison
Mizuno, Yosuke
de Lima Morais, David A.
Morikawa, Hiromasa
Morimoto, Mitsuru.
Moro, Kazuyo
Motakis, Efthymios
Motohashi, Hozumi
Mummery, Christine L.
Murata, Mitsuyoshi
Nagao-Sato, Sayaka
Nakachi, Yutaka
Nakahara, Fumio
Nakamura, Toshiyuki
Nakamura, Yukio
Nakazato, Kenichi
van Nimwegen, Erik
Ninomiya, Noriko
Nishiyori, Hiromi
Noma, Shohei
Nozaki, Tadasuke
Ogishima, Soichi
Ohkura, Naganari
Ohmiya, Hiroko
Ohno, Hiroshi
Ohshima, Mitsuhiro
Okada-Hatakeyama, Mariko
Okazaki, Yasushi
Orlando, Valerio
Ovchinnikov, Dmitry A.
Pain, Arnab
Passier, Robert
Patrikakis, Margaret
Persson, Helena
Piazza, Silvano
Prendergast, James G. D.
Rackham, Owen J. .
Ramilowski, Jordan A.
Rashid, Mamoon
Ravasi, Timothy
Rizzu, Patrizia
Roncador, Marco
Roy, Sugata
Rye, Morten B.
Saijyo, Eri
Sajantila, Antti
Saka, Akiko
Sakaguchi, Shimon
Sakai, Mizuho
Sato, Hiroki
Satoh, Hironori
Savvi, Suzana
Saxena, Alka
Schneider, Claudio
Schultes, Erik A.
Schulze-Tanzil, Gundula G.
Schwegmann, Anita
Sengstag, Thierry
Sheng, Guojun
Shimoji, Hisashi
Shimoni, Yishai
Shin, Jay W.
Simon, Christophe
Sugiyama, Daisuke
Sugiyama, Takaaki
Suzuki, Masanori
Suzuki, Naoko
Swoboda, Rolf K.
't Hoen, Peter A.C.
Tagami, Michihira
Takahashi, Naoko
Takai, Jun
Tanaka, Hiroshi
Tatsukawa, Hideki
Tatum, Zuotian
Thompson, Mark
Toyoda, Hiroo
Toyoda, Tetsuro
Valen, Eivind
van de Wetering, Marc
van den Berg, Linda M.
Verardo, Roberto
Vijayan, Dipti
Vorontsov, Ilya E.
Wasserman, Wyeth W.
Watanabe, Shoko
Wells, Christine A.
Winteringham, Louise N.
Wolvetang, Ernst
Wood, Emily J.
Yamaguchi, Yoko
Yamamoto, Masayuki
Yoneda, Misako
Yonekura, Yohei
Yoshida, Shigehiro
Zabierowski, Suzan E.
Zhang, Peter G.
Zhao, Xiaobei
Zucchelli, Silvia
Summers, Kim M.
Suzuki, Harukazu
Daub, Carsten O.
Kawai, Jun
Heutink, Peter
Hide, Winston
Freeman, Tom C.
Lenhard, Boris
Bajic, Vladimir B.
Taylor, Martin S.
Makeev, Vsevolod J.
Sandelin, Albin
Hume, David A.
Carninci, Piero
Hayashizaki, Yoshihide
Title The constrained maximal expression level owing to haploidy shapes gene content on the mammalian X chromosome
Journal name PLoS Biology   Check publisher's open access policy
ISSN 1545-7885
1544-9173
Publication date 2015-12-18
Sub-type Article (original research)
DOI 10.1371/journal.pbio.1002315
Open Access Status DOI
Volume 13
Issue 12
Total pages 48
Place of publication San Francisco, CA, United States
Publisher Public Library of Science
Language eng
Abstract X chromosomes are unusual in many regards, not least of which is their nonrandom gene content. The causes of this bias are commonly discussed in the context of sexual antagonism and the avoidance of activity in the male germline. Here, we examine the notion that, at least in some taxa, functionally biased gene content may more profoundly be shaped by limits imposed on gene expression owing to haploid expression of the X chromosome. Notably, if the X, as in primates, is transcribed at rates comparable to the ancestral rate (per promoter) prior to the X chromosome formation, then the X is not a tolerable environment for genes with very high maximal net levels of expression, owing to transcriptional traffic jams. We test this hypothesis using The Encyclopedia of DNA Elements (ENCODE) and data from the Functional Annotation of the Mammalian Genome (FANTOM5) project. As predicted, the maximal expression of human X-linked genes is much lower than that of genes on autosomes: on average, maximal expression is three times lower on the X chromosome than on autosomes. Similarly, autosome-to-X retroposition events are associated with lower maximal expression of retrogenes on the X than seen for X-to-autosome retrogenes on autosomes. Also as expected, X-linked genes have a lesser degree of increase in gene expression than autosomal ones (compared to the human/Chimpanzee common ancestor) if highly expressed, but not if lowly expressed. The traffic jam model also explains the known lower breadth of expression for genes on the X (and the Z of birds), as genes with broad expression are, on average, those with high maximal expression. As then further predicted, highly expressed tissue-specific genes are also rare on the X and broadly expressed genes on the X tend to be lowly expressed, both indicating that the trend is shaped by the maximal expression level not the breadth of expression per se. Importantly, a limit to the maximal expression level explains biased tissue of expression profiles of X-linked genes. Tissues whose tissue-specific genes are very highly expressed (e.g., secretory tissues, tissues abundant in structural proteins) are also tissues in which gene expression is relatively rare on the X chromosome. These trends cannot be fully accounted for in terms of alternative models of biased expression. In conclusion, the notion that it is hard for genes on the Therian X to be highly expressed, owing to transcriptional traffic jams, provides a simple yet robustly supported rationale of many peculiar features of X’s gene content, gene expression, and evolution.
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Q-Index Status Provisional Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Australian Institute for Bioengineering and Nanotechnology Publications
UQ Diamantina Institute Publications
 
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