Journal Article

CRISPR mutagenesis confirms the role of oca2 in melanin pigmentation in Astyanax mexicanus

Klaassen, H., Wang, Y., Adamski, K., Rohner, N. and Kowalko, J.E.

Record Number:
4135
Year:
2018
Journal:
Developmental Biology
Pages:
313-318
Volume:
441
Abstract:
Understanding the genetic basis of trait evolution is critical to identifying the mechanisms that generated the immense amount of diversity observable in the living world. However, genetically manipulating organisms from natural populations with evolutionary adaptations remains a significant challenge. Astyanax mexicanus exists in two interfertile forms, a surface-dwelling form and multiple independently evolved cave-dwelling forms. Cavefish have evolved a number of morphological and behavioral traits and multiple quantitative trait loci (QTL) analyses have been performed to identify loci underlying these traits. These studies provide a unique opportunity to identify and test candidate genes for these cave-specific traits. We have leveraged the CRISPR/ Cas9 genome editing techniques to characterize the effects of mutations in oculocutaneous albinism II (oca2), a candidate gene hypothesized to be responsible for the evolution of albinism in A. mexicanus cave populations. We generated oca2 mutant surface A. mexicanus. Surface fish with oca2 mutations are albino due to a disruption in the first step of the melanin synthesis pathway, the same step that is disrupted in albino cavefish. Hybrid offspring from crosses between oca2 mutant surface and cavefish are albino, definitively demonstrating the role of this gene in the evolution of albinism in this species. This research elucidates the role oca2 plays in pigmentation in fish, and establishes that this gene is solely responsible for the evolution of albinism in multiple cavefish populations. Finally, it demonstrates the utility of using genome editing to investigate the genetic basis of trait evolution.
Times Cited:
1
Related Records:
Hubbs, C.L. and Innes, W.T. (1936)Bridges, W. (1940)Gresser, E. B. and Breder, C. M. (1940)Breder, C. M. and Gresser, E. B. (1941)Breder, C. M. and Gresser, E. B. (1941)Breder, C. M. and Gresser, E. B. (1941)Breder, C. M. (1942)Osorio Tafall, B. F. (1943)Breder, C. M. (1943)Breder, C. M. (1943)Breder, C. M. (1944)Alvarez, J. (1946)Breder, C. M. and Rasquin, P. (1947)Breder, C. M. and Rasquin, P. (1947)Schlagel, S. R. and Breder, C. M. (1947)Alvarez, J. (1947)Rasquin, P. (1949)Luling, K. H. (1953)Luling, K. H. (1953)Luling, K. H. (1953)Stefanelli, A. (1954)Rasquin, P. and Rosenbloom, L. (1954)Stefanelli, A. (1954)Luling, K. H. (1954)Luling, K. H. (1954)Thines, G. (1954)Luling, K. H. (1955)Luling, K. H. (1955)Sadoglu, P. (1956)Thines, G. and Kahling, J. (1957)Sadoglu, P. (1957)Sadoglu, P. (1957)Cahn, P. H. (1958)Grobbel, G. and Hahn, G. (1958)Kahling, J. (1961)Luling, K. H. (1962)Burgers, A. C. J., Bennink, P. J. H. and van Oordt, G. J. (1963)Franck, A. (1964)Thines, G., Wolff-Van Ermengem, F., Boucquey, C. and Soffie, M. (1965)Boucquey, C., Thines, G. and Van Der Borght, C. (1965)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Peters, N. and Peters, G. (1966)Carmignani, M. P. A. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Reed, M. (1966)Sadoglu, P. (1967)Schemmel, C. (1967)Walters, V. and Liu, R. K. (1967)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Popper, A. N. and Tavolga, W. N. (1967)Carmignani, M. P. A. (1968)Wilkens, H. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Mattheij, J. A. and Sprangers, J. A. P. (1969)Sadoglu, P. and McKee, A. (1969)Weiss, B. A. (1969)Mattheij, J. A. (1969)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Weiss, B. and Martini, J. (1970)Gertychowa, R. (1970)Whitt, G. S. and Maeda, F. S. (1970)Gertychowa, R. (1970)Popper, A. N. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wiley, S. and Mitchell, R. W. (1971)Gertychowa, R. (1971)Popper, A. N. (1971)Wiley, S. and Mitchell, R. W. (1971)Wilkens, H. (1971)Zaccone, G. (1971)Thines, G. and Wissocq, N. (1972)Wilkens, H. and Burns, R. J. (1972)Avise, J. C. and Selander, R. K. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Zaccone, G. (1972)Wilkens, H. (1972)Thines, G. and LeGrain, J. M. (1973)Voneida, T. J. (1973)Schemmel, C. (1973)Yasuda, K. (1973)Zeitlin, S. M. (1973)Durand, J. P. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Mitchell, R. W. (1973)Schemmel, C. (1974)Schemmel, C. (1974)Chakraborty, R. and Nei, M. (1974)Sligar, C. (1974)Omura, Y. (1975)Sadoglu, P. (1975)Peters, N., Scholl, A. and Wilkens, H. (1975)Voneida, T. J. and Sligar, C. (1976)Sligar, C. and Voneida, T. J. (1976)Herwig, H. J. (1976)Herwig, H. J. (1976)Wilkens, H. (1976)Durand, J. P. (1976)Erckens, W. and Weber, F. (1976)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Yew, D. T. and Yoshihara, H. M. (1977)Zaccone, G. (1977)Wilkens, H. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (1977)Thines, G. and Weyers, M. (1978)Durand, J. P. (1978)Sadoglu, P. (1979)Wilkens, H., Peters, H. and Schemmel, C. (1979)Woodhead, A. D. and Achey, P. M. (1979)Durand, J. P. (1979)Schemmel, C. (1980)Weissert, R. (1980)Quinn, T. P. (1980)Wilkens, H. (1980)Wilkens, H. (1980)Campenhausen, C., Riess, I. and Weissert, R. (1981)Weissert, R. and Campenhausen, C. (1981)Reddell, J. R. (1981)Herwig, H. J. (1981)Jankowska, M. and Thines, G. (1982)Lamprecht, G. and Weber, F. (1982)Tabata, M. (1982)Erckens, W. and Martin, W. (1982)Erckens, W. and Martin, W. (1982)Rose, F. L. and Mitchell, R. W. (1982)Parzefall, J. (1983)Romero, A. (1983)Zilles, K., Tillmann, B. and Bennemann, R. (1983)Schuppa, M. (1984)Voneida, T. J. and Fish, S. E. (1984)Romero, A. (1984)Romero, A. (1984)Wilkens, H. (1984)Burchards, H., Dolle, A. and Parzefall, J. (1985)Lamprecht, G. and Weber, F. (1985)Teyke, T. (1985)Romero, A. (1985)Wilkens, H. (1985)Parzefall, J. (1986)Wilkens, H. and Huppop, K. (1986)De Fraipont, M. (1986)Fraipont, M. (1986)Hassan, E. S. (1986)De Fraipont, M. and Thines, G. (1986)De Fraipont, M. and Thines, G. (1986)Huppop, K. (1986)Romero, A. (1986)Wilkens, H. (1986)Wilkens, H. (1987)De Fraipont, M. (1987)De Fraipont, M. (1987)Huppop, K. (1987)Wilkens, H. (1988)Fricke, D. (1988)De Fraipont, M. (1988)Teyke, T. (1988)Huppop, K. (1988)Fack, H. and Wilkens, H. (1989)Langecker, T. G. (1989)Fricke, D. and Parzefall, J. (1989)Hassan, E. S. (1989)Teyke, T. (1989)Huppop, K. (1989)Klimpel, B. and Parzefall, J. (1990)Parzefall, J. and Fricke, D. (1990)Peters, N., Schmidt, W. and Fricke, D. (1990)Langecker, T. G. (1990)Abdel-Latif, H., Hassan, E. S. and von Campenhausen, C. (1990)Yokoyama, R. and Yokoyama, S. (1990)Yokoyama, R and Yokoyama, S (1990)Teyke, T. (1990)Huppop, K. (1991)Parzefall, J. and Fricke, D. (1991)Campenhausen, C. (1991)Langecker, T. G., Wilkens, H. and Junge, P. (1991)Riedel, G. and Krug, L. (1991)Huppop, K. and Wilkens, H. (1991)Wilkens, H. (1992)Parzefall, J. (1992)Parzefall, J. (1992)Wilkens, H. and Meyer, M. (1992)Lamprecht, G. and Weber, F. (1992)Langecker, T. G. and Longley, G. (1992)Hassan, E. S., Abdel-Latif, H. and Biebricher, R. (1992)De Fraipont, M. (1992)Parzefall, J. (1993)Peters, N., Schacht, V., Schmidt, W. and Wilkens, H. (1993)Langecker, T. G. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Langecker, T. G., Schmale, H. and Wilkens, H. (1993)Hoffman, S. and Hausberg, C. (1993)Borowsky, R. (1994)Teyke, T. and Schaerer, S. (1994)Langecker, T. G., Neumann, B., Hausberg, C. and Parzefall, J. (1995)Langecker, T. G., Wilkens, H. and Schmale, H. (1995)Yokoyama, S., Meany, A., Wilkens, H. and Yokoyama, R. (1995)Borowsky, R. (1996)Behrens, M., Langecker, T.G., Wilkens, H. and Schmale, H. (1997)Riedel, G. (1997)Riedel, G. and Krug, L. (1997)Borowsky, R. and Espinasa, L. (1997)Wilkens, H. (1998)Jeffery, WR and Martasian, DP (1998)Behrens, M, Wilkens, H and Schmale, H (1998)Contreras-Balderas, S. and Lozano-Vilano, M.D.L. (1998)Kullander, S. O. (1999)Baker, CF and Montgomery, J (1999)Espinasa, L. and Borowsky, R. (2000)Jeffery, W. R., Strickler, A.G., Guiney, S., Heyser, D.G. and Tomarev, S.I. (2000)Yamamoto, Y. and Jeffery, W. R. (2000)Ford, D.C. (2000)Espinasa, L. and Borowsky, R. (2001)Jeffery, W. R. (2001)Strickler, A.G., Yamamoto, Y. and Jeffery, W. R. (2001)Boudriot, F and Reutter, K (2001)Montgomery, J.C., Coombs, S. and Baker, C.F. (2001)Romero, A., Jeffery, W.R. and Yamamoto, Y. (2002)Berg, A. and Watson, G.M. (2002)Dowling, TE, Martasian, DP and Jeffery, WR (2002)Strickler, AG, Famuditimi, K and Jeffery, WR (2002)Krejca, J. (2002)Borowsky, RL and Wilkens, H (2002)Sarma, SSS, Lopez-Romulo, A and Nandini, S (2003)Wilkens, H. and Strecker, U. (2003)Contreras-Balderas, S, Almada-Villela, P, Lozano-Vilano, M de L and Garcia-Ramirez, ME (2003)Strecker, U. (2003)Porter, M.L. and Crandall, K.A. (2003)Strecker, U., Bernatchez, L. and Wilkens, H. (2003)McCauley, DW, Hixon, E and Jeffery, WR (2004)Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ. (2006)Protas, M., Conrad, M., Gross, J.B., Tabin, C. and Borowsky, R.L. (2007)Protas, M, Tabansky, I, Conrad, M, Gross, JB, Vidal, O, Tabin, C and Borowsky, RL (2008)Salin, K, Voituron, Y, Colson, C and Hervant, F (2008)Gross, J.B., Protas, M., Conrad, M., Scheid, P.E., Vidal, O., Jeffery, W.R., Tabin, C. and others (2008)Kowalko, J, Gross, JB, Protas, M, Borowsky, RL and Tabin, C (2009)Jeffery, WR (2009)Salin, K., Voituron, Y., Mourin, J. and Hervant, F. (2010)Esquivel-Bobadilla, S (2011)Kowalko, J, Rohner, N, Borowsky, RL and Tabin, C (2011)Bradic, M, Beerli, P and Borowsky, RL (2011)Salin, K, Voituron, Y, Mourin, J and Hervant, F (2011)Yamamoto, Y. and Jeffery, W.R. (2011)Kish, P.E., Bohnsack, B.L., Gallina, D., Kasprick, D.S. and Kahana, A. (2011)Gross, J.B. (2012)Bradic, M., Beerli, P., Garcia-de Leon, F. J., Esquivel-Bobadilla, S. and Borowsky, R. L. (2012)Protas, M. and Jeffery, W. R. (2012)Hervant, F. (2012)Wilkens, H. (2012)Trontelj, P. (2012)Idda, M.L., Bertolucci, C., Vallone, D., Gothilf, Y., Sánchez-Vázquez, F.J. and Foulkes N.S. (2012)Dufton, M, Hall, BK and Franz-Odendaal, T. (2012)Jeffery, W.R. (2012)Beale, A., Guibal, C., Tamai, T. K., Klotz, L., Cowen, S., Peyric, E., Reynoso, V. H., Yamamoto, Y. and Whitmore, D. (2013)Elliott, William R. (2013)Beale, A. (2013)Kowalko, J.E., Rohner, N., Rompani, S.B., Peterson, B.K., Linden, T.A., Yoshizawa, M., Kay, E.H., Weber, J., Hoekstra, H.E., Jeffery, W.R., Borowsky, R. and Tabin, C.J. (2013)Rohner, N., Jarosz, D.F., Kowalko, J.E., Yoshizawa, M., Jeffery, W.R., Borowsky, R.L., Lindquist, S. and Tabin, C.J. (2013)Rohner, N (2013)Kowalko, J., Rohner, N., Linden, T.A., Rompani S.B., Warren, W.C., Borowsky, R., Tabin, C.J., Jeffery, W.R. and Yoshizawa M. (2013)Bradic, M., Teotonio, H. and Borowsky, R. L. (2013)Gross, J.B., Furterer, A., Carlson, B.M. and Stahl, B.A. (2013)Stahl, B. A. and Gross, J. B. (2013)Stahl, AL (2013)Pennisi, E. (2013)Pazza, R (2013)Bibliowicz, J., Alie, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Pere, S. and Retaux, S. (2013)Atukorala, A. D. S., Hammer, C., Dufton, M. and Franz-Odendaal, T. A. (2013)Elliott, W.R. (2014)Gross, J.B., Krutzler, A.J. and Carlson, B.M. (2014)Espinasa, L., Bartolo, N.D. and Newkirk, C.E. (2014)Atukorallaya, D. and Franz-Odendaal, T. (2014)McGaugh, S.E., Gross, J.B., Aken, B., Blin, M., Borowsky, R., Chalopin, D., Hinaux, H., Jeffery, W.R., Keene, A., Ma, L., Minx, P., Murphy, D., O'Quin, K.E., Retaux, S., Rohner, N., Searl, S.M., Stahl, B.A., Tabin, C., Volff, J.N., Yoshizawa M, Warren WC. (2014)Atukorala, A. D. S. and Franz-Odendaal, T. A. (2014)Moran, D., Softley, R. and Warrant, E.J. (2014)Fumey, J. (2015)Caballero-Hernandez, O., Hernandez-Patricio, M., Sigala-Regalado, I., Morales-Malacara, J. B. and Miranda-Anaya, M. (2015)Aspiras, A.C., Rohner, N., Martineau, B., Borowsky, R.L. and Tabin, C.J. (2015)Bradic, M, Rohner, N, Tabin, C and Borowsky, R. (2015)Stahl, Bethany A. and Gross, Joshua B. (2015)Rohner, N (2015)Riddle, M and Tobin, C. J. (2015)Stahl, B. A., Ma, L and Gross, J. B. (2015)Yoshizawa, Masato, Robinson, Beatriz G., Duboue, Erik R., Masek, Pavel, Jaggard, James B., O'Quin, Kelly E., Borowsky, Richard L., Jeffery, William R. and Keene, Alex C. (2015)Jaggard, J. B. (2015)Stemmer, M., Schuhmacher, L.-N., Foulkes, N.S., Bertolucci, C. and Wittbrodt, J. (2015)Devos, Lucie, Alie, A. and Retaux, S (2015)Carlson, B.M., Onusko, S.W. and Gross, J.B. (2015)Silva, D. M. Z. A., Utsunomia, R., Pansonato-Alves, J.C., Oliveira, C. and Foresti, F. (2015)McGaugh, S. E. (2015)Dufton, Megan and Franz-Odendaal, Tamara A. (2015)Moran, D., Softley, R. and Warrant, E.J. (2015)Hinaux, H., Blin, M., Fumey, J., Legendre, L., Heuze, A., Casane, D. and Retaux, S. (2015)Beale, A., Whitmore, D. and Moran, D. (2016)Beale, A. D. and Whitmore, D. (2016)Rohner, Nicolas (2016)Gross, J.B., Stahl, B.A., Powers, A.K. and Carlson, B.M. (2016)Aspiras, A., Tabin, C. and Rohner, N. (2016)Pennisi, E. (2016)Schmitter-Soto, JJ (2016)Pennisi, E (2016)Yoshizawa, M., Settle, A., Macaspac, C., Fernandes, V. Yoshida, M. and Keene, A. (2016)Keene, A.C., Yoshizawa, M. and McGaugh, S.E. (2016)Foulkes, N. S., Whitmore, D., Vallone, D and Bertolucci, C. (2016)Retaux, S., Alie, A., Blin, M., Devos, L., Elipot, Y. and Hinaux, H. (2016)Carlson, B.M. and Gross, J.B. (2016)Casane, D. and Retaux, S. (2016)O'Quin, Kelly and McGaugh, Suzanne E. (2016)Atukorala, A. D. S. and Franz-Odendaal, Tamara A. (2016)Fumey J, Hinaux H, Noirot C, Thermes C, Re´ taux S, Casane D. (2017)Lyon, A., Powers, A. K., Gross, J. B. and O'Quin, K. E. (2017)Gross, J. B. (2017)Riddle, M (2017)Kaplan, S.A., Powers, A.K. and Gross, J.B. (2017)Jaggard, J. B., Robinson, B. G., Stahl, B, Oh, I, Masek, P, Yoshizawa, M and Keene, A. (2017)Krishnan, J and Rohner, N (2017)Alvarado, C.G. (2017)Stahl, B (2017)Schmitter-Soto, JJ (2017)Stahl, B.A. and Gross, J.B. (2017)Yoshizawa, M (2017)Riddle, M. R.; Tabin, C. J (2017)Jaggard, J. B. (2017)Wilkens, H. and Strecker, U. (2017)Hinaux, H, Recher, G, Alie, A., Legendre, L, Blin, M. and Retaux, S (2017)Torres-Paz, J (2017)Riddle, M (2017)Frøland Steindal, I.V., Beale, A.D., Yamamoto, Y. and Whitmore, D. (2018)Devi, A., Atukorala, S. and Franz-Odendaal, T.A. (2018)Retaux, S. (2018)Blin, M., Tine, E., Meister, L., Elipot, Y., Bibliowicz, J., Espinasa, L. and Rétaux, S. (2018)Espinasa, L. (2018)Ornelas-García, P,. Pajares, S., Sosa-Jiménez, V.M., Rétaux, S. and Miranda-Gamboa, R.A. (2018)Espinasa, L., Legendre, L., Fumey, J., Blin, M., Rétaux, S. and Espinasa, M. (2018)Powers, A.K., Kaplan, S.A., Boggs, T.E. and Gross, J. (2018)Sovrano, V.A., Potrich, D., Foà, A. and Bertolucci, C. (2018)Mirande, J.M. (2018)Carlson, B.M. and Gross, J.B. (2018)Borowsky, R. (2018)Sears, C.R. and Gross, J.B. (2018)Tabin, J.A., Aspiras, A., Martineau, B., Riddle, M., Kowalko, J. Borowsky, R. Rohner, N. and Tabin, C.J. (2018)Stah, B.A., Sears, C.R., Ma, L., Perkins, M. and Gross, J.B. (2018)Borowsky, R., Luk, A., He, X.J. and Kim, R.S. (2018)Powers, A.K., Boggs, T.E. and Gross, J.B. (2018)Riddle, M.R., Aspiras, A.C., Gaudenz, K., Peuß, R., Sung, J.Y., Martineau, B., Peavey, M., Box, A.C., Tabin, J.A., McGaugh, S., Borowsky, R., Tabin, C.J. and Rohner, N. (2018)Garita-Alvarado, C.A., Barluenga, M. and Ornelas-García, C.P. (2018)Rohner, N. (2018)Pazza, R., Dergam, J.A. and Kavalco, K.F. (2018)Yoshizawa, M., Settle, A., Hermosura, M.C., Tuttle, L.J., Cetraro, N., Passow, C.N. and McGaugh, S.E. (2018)Riddle, M.R., Boesmans, W., Caballero, O, Kazwiny, Y. and Tabin,C.J. (2018)Fernandes, V.F.L., Macaspac, C., Lu, L. and Yoshizawa, M. (2018)Riddle, M., Martineau, B., Peavey, M. and Tabin, C. (2018)Kopp, J., Avasthi, S. and Espinasa, L. (2018)Jaggard, J.B., Stahl, B.A., Lloyd, E., Prober, D.A., Duboue, E.R. and Keene, A.C. (2018)Kling, J. (2018)Ojha, A. and Watve, M. (2018)Chin, J.S.R., Gassant, C.E., Amaral, P.M., Lloyd, E., Stahl, B.A., Jaggard, J.B., Keene, A.C. and Duboue, E.R. (2018)Gore, A., Jeffery, W., Retaux, S. and Rohner, N. (2018)Gore, A.V., Rohner, N., Rétaux, S. and Jeffery, W.R. (2018)Stern, D.B and Crandall, K.A. (2018)Ma, L., Strickler, A.G., Parkhurst, A., Yoshizawa, M., Shi, J. and Jeffery, W.R. (2018)Torres-Paz,J., Hyacinthe, C., Pierre, C., Retaux, S. (2018)Alie, A., Devos, L., Torres-Paz, J., Prunier, L., Boulet, F., Blin, M., Elipot, Y. and Retaux, S. (2018)Xiong, S., Krishnan, J., Peuß, F. and Rohner, N. (2018)Ren, X.Y., Hamilton, N., Müller, F. and Yamamoto, Y. (2018)Elliott, W.R. (2018)Devitsina, G.V. and Golovkina, T.V. (2018)Carlson, B.M., Klingler, I.B., Meyer, B.J. and Gross, J.B. (2018)Klaassen, H., Wang, Y., Adamski, K., Rohner, N. and Kowalko, J.E. (2018)Fumey, J., Hinaux, H., Noirot, C., Thermes, C., Rétaux, S. and Casane, D. (2018)Rohner, N. (2018)Gross, J.B., Weagley, J., Stahl, B.A., Ma, L., Espinasa, L. and McGaugh, S.E. (2018)Pennisi, E. (2019)