- Email: [email protected]
Evolution: He Who Grabs Too Much Loses All
Dispatch R961
12.
13.
14.
15.
of anterogradely transported Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 285, 54–72. Gilbert, C.D., and Li, W. (2013). Top-down influences on visual processing. Nat. Rev. Neurosci. 14, 350–363. Schroeder, C.E., and Lakatos, P. (2009). Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 32, 9–18. Douglas, R.J., Martin, K.A.C., and Whitteridge, D. (1989). A canonical microcircuit for neocortex. Neural Comput. 1, 480–488. Nelson, S. (2002). Cortical microcircuits: diverse or canonical? Neuron 1, 19–27.
16. Shipp, S. (2005). The importance of being agranular: a comparative account of visual and motor cortex. Phil. R. Soc. Lond. B 360, 797–814. 17. Mitchell, J.F., Sundberg, K.A., and Reynolds, J.H. (2007). Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55, 131–141. 18. Steinmetz, N.A., and Moore, T. (2012). Lumping and splitting the neural circuitry of visual attention. Neuron 73, 410–412. 19. Harris, K.D., and Thiele, A. (2011). Cortical state and attention. Nat. Rev. Neurosci. 12, 509–523.
Evolution: He Who Grabs Too Much Loses All Polyploidy can result in both evolutionary dead-ends and successful evolutionary transitions. A pair of recent papers indicates that adapting meiosis is a necessary step on the way to becoming a successful polyploid. Eric Jenczewski1,2 Polyploid species can be viewed as ‘hopeful monsters’. They originate via chromosome doubling, a severe macromutation that triggers additional chromosomal, genetic and epigenetic changes especially when it is associated with interspecific hybridization (i.e., allopolyploids [1]). Polyploidy can produce immediate shifts in the range of environmental conditions that an organism can tolerate [1–3]; this greater resilience being enabled by both the original genetic attributes [4] and the innovative or transgressive phenotypes [5,6] that are provided by polyploidy. Polyploids are indeed widespread among plants [7] and fungi [8], and they are commonplace among certain groups of insects, fish and amphibians [2]. However, all these proofs of success do not mean that polyploidy is essentially beneficial nor that polyploids achieve perfection overnight. To the contrary, newly formed polyploids face significant hurdles from the outset and those that are unable to meet these challenges are likely to be ‘hopeless’ and condemned to certain death. A highly topical issue is thus to understand which physiological or cellular functions need to be adapted to polyploidy. This is the question addressed by the Bomblies lab in two recent papers, including one in this issue of Current Biology [9,10]. These
papers, particularly the last one, indicate that ensuring faithful chromosome segregation during meiosis is key to ensure the hopefulness of an autopolyploid monster. Yant et al. [10] used full genomic scans to compare diploid and autotetraploid plants of Arabidopsis arenosa (Figure 1), a very close relative to Arabidopsis thaliana, and identify candidate targets of natural selection during the establishment of the autotetraploid lineage. They looked for genes showing increased genetic differences between diploid and autotetraploid individuals as compared to a genome-wide average. The rationale for this is that most evolutionary processes (such as population demography, genetic drift, gene flow) affect all loci in a genome equally, whereas natural selection acts on specific loci. Through this approach, Yant et al. [10] identified 44 candidate selected genes in autotetraploid A. arenosa, among which 8 were shown to play a role during meiosis in A. thaliana. This is an unexpectedly clear overrepresentation of meiotic genes. What could be the reason? In most sexually reproducing organisms, correct chromosome segregation during meiosis requires pairs of homologous chromosomes to be held together by chiasmata, the stable connections produced by the combined effect of sister-chromatid cohesion and inter-chromosomal
20. Carandini, M. (2012). From circuits to behavior: a bridge too far? Nat. Neurosci. 15, 507–509.
Department of Psychology, College of Arts and Science, Vanderbilt University, Wilson Hall 008, 111 21st Avenue South, Nashville, TN 37203, USA. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2013.09.010
reciprocal recombination (i.e., the crossovers). In polyploid species, the presence of multiple sets of chromosomes makes this process more demanding. As every chromosome has more than a single possible match, multiple chiasmatic associations can readily be formed, resulting in an unequal distribution of homologues whenever the multivalents are asymmetrically orientated on the metaphase I plate [11]. Multivalents thus impose a heavy burden of newly formed polyploids as they contribute to umbalanced gamete formation, aneuploidies and reduced fertility [12]. Autopolyploids are particularly at risk here because of their chromosome content. Being derived from within a single parental species, all recombining partners in an autopolyploid share the same degree of kinship and they are thus especially prone to multivalent formation [11,12]. This is exactly what Yant et al. [10] observed in artificially induced autotetraploids of A. arenosa. These newly generated autotetraploids show conspicuous meiotic abnormalities and reduced pollen fertility. By contrast, natural autotetraploid accessions mainly form bivalents at metaphase I (see also [13]) and display high pollen fertility [10]. Thus, reproductive fitness is not innate in autotetraploid A. arenosa but it rather required ‘‘naturally evolved solution(s)’’ to polyploidy-associated challenges [10]. Although identification of 36 non-meiotic candidate selected genes demonstrates that many other vital biological processes require adaptive responses to genome doubling [9,14], the overrepresentation of candidate selected meiotic genes in A. arenosa suggests that one of the biggest stumbling blocks to the successful establishment of newly formed
Current Biology Vol 23 No 21 R962
Figure 1. Arabidopsis arenosa. Autotetreploid Arabidopsis arenosa from eastern Austria, along the Danube river. (Photo credits: Roswitha Schmickl and Marcus Koch.)
polyploids is their initial inability to properly segregate chromosomes during meiosis. Meiosis in natural autotetraploid A. arenosa shows another important idiosyncrasy. Although bivalents are formed at metaphase I, they consist of randomly chosen pairs of homologues; all possible allelic combinations at a given locus are produced in equal frequencies in autotetraploid A. arenosa [9]. This pattern is diagnostic for tetrasomic inheritance and indicates that A. arenosa has ‘‘cytologically, but not genetically diploidized meiosis’’ [9]. Although A. arenosa is no exception in this respect [4,12], it represents a promising model to understand how this can occur. Yant et al. [10] observed a significant reduction of crossover frequencies in natural autotetraploids compared to diploids and the corresponding colchicine-induced tetraploids. Most bivalents in the natural autotetraploids are held by single chiasmata (see also [13]) whereas a majority of bivalents are bound by at least two chiasmata in diploids and neotetraploids. This result makes much sense, because there is no opportunity for multivalent formation when all chromosomes undergo one (obligatory) crossover only. By contrast, the colchicine-induced tetraploid that ‘grabs too much loses all’ because increased crossover frequencies result in increased meiotic abnormalities. In fact, Yant et al. [10] do far more than just support the longstanding idea that reduced crossover frequency helps to improve chromosome segregation and fertility in autopolyploids. They also shed new
light on, or offer new opportunities to investigate the mechanistic and evolutionary origin of this adaptation. The candidate selected meiotic genes identified in [10] represent a remarkably limited set of functions involved in the early steps of meiotic recombination (AaPRD3, AaASY1, AsASY3, AaZYP1a, AaZYP1b) and sister-chromatid cohesion (AaSYN1, AaSMC6). Owing to its small sample size, this list makes it possible to test whether the selected variants contribute effectively to reduce crossover frequency. The list also raises questions as to why such a specific sample of interrelated genes has been targeted, when meiotic recombination depends on a far wider range of factors. Does this mean that the earliest variant to get selected has set a path that the latter have to follow to keep forging ahead? Or are there preferential targets that one might not see at first glance? In this respect, it is noteworthy that ASY1 has also been hypothesized to contribute to the cytological diploidization of allopolyploid wheat [15]. Notwithstanding this last point, the work of Yant et al. [10] now offers the possibility to test whether the same set of genes has been targeted by natural selection in another cytologically, but not genetically diploidized autopolyploid lineage. One may finally ask whether selection has acted on alleles already segregating within the diploid populations or whether the variants were selected right after they originated in the autotetraploid population(s). The first answer is correct for AaASY1, for which the allele which is almost fixed in the tetraploids
occurs at a very low frequency in the diploids [9]. This result suggests that natural autotetraploid A. arenosa may have originated from the union of parental genotypes fortuitously endowed with beneficial/potentiating mutations already present in the diploid populations. Further investigations are needed to understand whether the same holds true for the other candidate selected meiotic genes and thus how such polygenic architecture has evolved in natural autotetraploid A. arenosa. Despite considerable empirical observations and theoretical predictions, the cytological diploidization of polyploid species has remained a mystery for a long time. The work of Yant et al. [10], together with the molecular characterization of the Ph1 locus in wheat [16], has begun to fill this gap. One would, however, be wrong to believe that reduced chiasma frequency is always a prerequisite for the establishment of a new polyploid species [17–19]. In fact, and as might be expected, hopeful polyploid monsters most likely have more than one trick up their sleeves! References 1. Madlung, A. (2013). Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110, 99–104. 2. Otto, S.P., and Whitton, J. (2000). Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437. 3. Van de Peer, Y., Maere, S., and Meyer, A. (2009). The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10, 725–732. 4. Parisod, C., Holderegger, R., and Brochmann, C. (2010). Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17. 5. Ni, Z., Kim, E.D., Ha, M., Lackey, E., Liu, J., Zhang, Y., Sun, Q., and Chen, Z.J. (2009). Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327–331. 6. Chao, D.Y., Dilkes, B., Luo, H., Douglas, A., Yakubova, E., Lahner, B., and Salt, D.E. (2013). Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341, 658–659. 7. Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100. 8. Albertin, W., and Marullo, P. (2012). Polyploidy in fungi: evolution after whole-genome duplication. Proc. Biol. Sci. 279, 2497–2509. 9. Hollister, J.D., Arnold, B.J., Svedin, E., Xue, K.S., Dilkes, B.P., and Bomblies, K. (2012). Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 8, e1003093. 10. Yant, L., Hollister, J.D., Wright, K.M., Arnold, B.J., Higgins, J.D., Franklin, F.C.H., and Bomblies, K. (2013). Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23, 2151–2156. 11. Grandont, L., Jenczewski, E., and Lloyd, A. (2013). Meiosis and its deviations in polyploid plants. Cytogenet. Genome Res. 140, 171–184.
Dispatch R963
12. Ramsey, J., and Schemske, D.W. (2002). Neopolyploidy in flowering plants. Annu. Rev. Ecol. Systemat. 33, 589–639. 13. Carvalho, A., Delgado, M., Bara˜o, A., Frescatada, M., Ribeiro, E., Pikaard, C., Viegas, W., and Neves, N. (2010). Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa. Sex Plant Reprod. 23, 29–37. 14. Storchova, Z., Breneman, A., Cande, J., Dunn, J., Burbank, K., O’Toole, E., and Pellman, D. (2006). Genome-wide genetic analysis of polyploidy in yeast. Nature 443, 541–547. 15. Boden, S.A., Langridge, P., Spangenberg, G., and Able, J.A. (2009). TaASY1 promotes
homologous chromosome interactions and is affected by deletion of Ph1. Plant J. 57, 487–497. 16. Griffiths, S., Sharp, R., Foote, T.N., Bertin, I., Wanous, M., Reader, S., Colas, I., and Moore, G. (2006). Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439, 749–752. 17. Hazarika, M.H., and Rees, H. (1967). Genotypic control of chromosome behaviour in rye X. Chromosome pairing and fertility in autotetraploids. Heredity 22, 317–332. 18. Crowley, J.G., and Rees, H. (1968). Fertility and selection in tetraploid Lolium. Chromosoma 24, 300–308.
Cell Biology: Cytoskeleton Network Topology Feeds Back on Its Regulation Many cell functions rely on microtubule dynamics and ordering. Two recent studies show that microtubule severing by katanin plays an overbearing role in this process and is primarily regulated at microtubule crossovers. Olivier Hamant By showing how microtubule crossovers are at a central position in the control of cytoskeleton ordering, and by providing a regulatory mechanism underlying this control, the work by Zhang et al. [1] in this issue and Wightman et al. [2] published recently in Current Biology illustrates how plant research provides important new findings that are relevant to cell biology in all kingdoms, with implications in development and biomedical research, too. Understanding the regulation of microtubule dynamics is crucial to many biological processes. This is probably most obvious in plants — in this kingdom, growth is driven by turgor pressure, and the mechanical properties of the cell wall constrain its rate and direction. Because microtubules control the deposition of cellulose [3], and thus the mechanical anisotropy of cell walls, any defect in microtubule behavior is translated into an abnormal macroscopic cell and tissue shape [4]. Most remarkably, when microtubules are depolymerized, aerial plant organs become spherical and cells resemble soap bubbles [5]. Mutants with disorganized microtubules also exhibit isotropic growth, and among the known regulators, the microtubule severing protein katanin has emerged as
one of the main controlling factors. In fact, one of the katanin alleles in Arabidopsis is called botero, referencing the artist’s work reflecting the rather obese and thus isotropic geometry of the corresponding mutant phenotype [6]. Katanin was originally purified in extracts from sea urchin eggs. Since then, this AAA ATPase has been found in all eukaryotes and acts as an heterodimer, with the 60 kDa katanin subunit displaying the catalytic activity, and the 80 kDa WD40-repeat counterpart displaying a regulatory role [7]. Importantly, while the function of katanin was initially associated with centrosomal microtubules, there is now evidence that this role is also relevant to non-centrosomal microtubules. This is not only illustrated by the work conducted in plants — katanin is also involved in the control of axonal growth [8] and cell migration [9]. Katanin has also been proposed to increase the number of short microtubule fragments near meiotic chromatin to compensate for their rather inefficient nucleation in this context [10]. Therefore, the work that is highlighted here [1,2] consolidates some ideas and provides a number of predictions that may change the way we understand microtubule ordering in all eukaryotes. Briefly, Zhang et al. [1] show that katanin activity is triggered through
19. Brubaker, C.L., Paterson, A.H., and Wendel, J.F. (1999). Comparative genetic mapping of allotetraploid cotton and its diploid progenitors. Genome 42, 184–203.
1INRA, UMR1318, Institut Jean-Pierre Bourgin, RD10, F-78000 Versailles, France. 2AgroParisTech, Institut Jean-Pierre Bourgin, RD10, F-78000 Versailles, France. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2013.09.023
one dominant mechanism: cutting microtubules where they cross each other. Microtubule severing had previously been shown to occur preferentially at microtubule crossovers in a seminal article [11]. The work by Zhang et al. thus narrows down the molecular mechanism to only one predominant factor — katanin. In particular, they show that this enzyme localizes to microtubule crossovers and that in a katanin mutant, severing at crossovers is completely absent (Figure 1). Interestingly, a quantitative analysis of the corresponding kinetics highlights that longer-lived crossovers are more prone to severing than early ones, demonstrating that microtubule crossovers act both as a spatial and temporal regulator of severing [1]. This provides a feedback loop in which microtubule severing by katanin promotes the organization of the microtubule network, which in turn, through the amount, position and age of crossovers, regulates katanin activity. Because of their prevailing role in controlling microtubule organization, crossovers in the microtubule network emerge as a central regulatory point in plant cell biology. The work by Wightman, et al. [2] illustrates this idea by providing a new regulatory module that relies on microtubule crossovers. The authors notably show that the presence of highly aligned microtubule bundles in the spiral2 mutant is due to the inhibition of severing by SPR2, a previously identified microtubule-associated protein (MAP). More strikingly, they found that SPR2 accumulates at microtubule crossovers, where it prevents severing locally (Figure 1). Interestingly, this activity is also modulated in different cell types — the increased severing
12.
13.
14.
15.
of anterogradely transported Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 285, 54–72. Gilbert, C.D., and Li, W. (2013). Top-down influences on visual processing. Nat. Rev. Neurosci. 14, 350–363. Schroeder, C.E., and Lakatos, P. (2009). Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 32, 9–18. Douglas, R.J., Martin, K.A.C., and Whitteridge, D. (1989). A canonical microcircuit for neocortex. Neural Comput. 1, 480–488. Nelson, S. (2002). Cortical microcircuits: diverse or canonical? Neuron 1, 19–27.
16. Shipp, S. (2005). The importance of being agranular: a comparative account of visual and motor cortex. Phil. R. Soc. Lond. B 360, 797–814. 17. Mitchell, J.F., Sundberg, K.A., and Reynolds, J.H. (2007). Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55, 131–141. 18. Steinmetz, N.A., and Moore, T. (2012). Lumping and splitting the neural circuitry of visual attention. Neuron 73, 410–412. 19. Harris, K.D., and Thiele, A. (2011). Cortical state and attention. Nat. Rev. Neurosci. 12, 509–523.
Evolution: He Who Grabs Too Much Loses All Polyploidy can result in both evolutionary dead-ends and successful evolutionary transitions. A pair of recent papers indicates that adapting meiosis is a necessary step on the way to becoming a successful polyploid. Eric Jenczewski1,2 Polyploid species can be viewed as ‘hopeful monsters’. They originate via chromosome doubling, a severe macromutation that triggers additional chromosomal, genetic and epigenetic changes especially when it is associated with interspecific hybridization (i.e., allopolyploids [1]). Polyploidy can produce immediate shifts in the range of environmental conditions that an organism can tolerate [1–3]; this greater resilience being enabled by both the original genetic attributes [4] and the innovative or transgressive phenotypes [5,6] that are provided by polyploidy. Polyploids are indeed widespread among plants [7] and fungi [8], and they are commonplace among certain groups of insects, fish and amphibians [2]. However, all these proofs of success do not mean that polyploidy is essentially beneficial nor that polyploids achieve perfection overnight. To the contrary, newly formed polyploids face significant hurdles from the outset and those that are unable to meet these challenges are likely to be ‘hopeless’ and condemned to certain death. A highly topical issue is thus to understand which physiological or cellular functions need to be adapted to polyploidy. This is the question addressed by the Bomblies lab in two recent papers, including one in this issue of Current Biology [9,10]. These
papers, particularly the last one, indicate that ensuring faithful chromosome segregation during meiosis is key to ensure the hopefulness of an autopolyploid monster. Yant et al. [10] used full genomic scans to compare diploid and autotetraploid plants of Arabidopsis arenosa (Figure 1), a very close relative to Arabidopsis thaliana, and identify candidate targets of natural selection during the establishment of the autotetraploid lineage. They looked for genes showing increased genetic differences between diploid and autotetraploid individuals as compared to a genome-wide average. The rationale for this is that most evolutionary processes (such as population demography, genetic drift, gene flow) affect all loci in a genome equally, whereas natural selection acts on specific loci. Through this approach, Yant et al. [10] identified 44 candidate selected genes in autotetraploid A. arenosa, among which 8 were shown to play a role during meiosis in A. thaliana. This is an unexpectedly clear overrepresentation of meiotic genes. What could be the reason? In most sexually reproducing organisms, correct chromosome segregation during meiosis requires pairs of homologous chromosomes to be held together by chiasmata, the stable connections produced by the combined effect of sister-chromatid cohesion and inter-chromosomal
20. Carandini, M. (2012). From circuits to behavior: a bridge too far? Nat. Neurosci. 15, 507–509.
Department of Psychology, College of Arts and Science, Vanderbilt University, Wilson Hall 008, 111 21st Avenue South, Nashville, TN 37203, USA. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2013.09.010
reciprocal recombination (i.e., the crossovers). In polyploid species, the presence of multiple sets of chromosomes makes this process more demanding. As every chromosome has more than a single possible match, multiple chiasmatic associations can readily be formed, resulting in an unequal distribution of homologues whenever the multivalents are asymmetrically orientated on the metaphase I plate [11]. Multivalents thus impose a heavy burden of newly formed polyploids as they contribute to umbalanced gamete formation, aneuploidies and reduced fertility [12]. Autopolyploids are particularly at risk here because of their chromosome content. Being derived from within a single parental species, all recombining partners in an autopolyploid share the same degree of kinship and they are thus especially prone to multivalent formation [11,12]. This is exactly what Yant et al. [10] observed in artificially induced autotetraploids of A. arenosa. These newly generated autotetraploids show conspicuous meiotic abnormalities and reduced pollen fertility. By contrast, natural autotetraploid accessions mainly form bivalents at metaphase I (see also [13]) and display high pollen fertility [10]. Thus, reproductive fitness is not innate in autotetraploid A. arenosa but it rather required ‘‘naturally evolved solution(s)’’ to polyploidy-associated challenges [10]. Although identification of 36 non-meiotic candidate selected genes demonstrates that many other vital biological processes require adaptive responses to genome doubling [9,14], the overrepresentation of candidate selected meiotic genes in A. arenosa suggests that one of the biggest stumbling blocks to the successful establishment of newly formed
Current Biology Vol 23 No 21 R962
Figure 1. Arabidopsis arenosa. Autotetreploid Arabidopsis arenosa from eastern Austria, along the Danube river. (Photo credits: Roswitha Schmickl and Marcus Koch.)
polyploids is their initial inability to properly segregate chromosomes during meiosis. Meiosis in natural autotetraploid A. arenosa shows another important idiosyncrasy. Although bivalents are formed at metaphase I, they consist of randomly chosen pairs of homologues; all possible allelic combinations at a given locus are produced in equal frequencies in autotetraploid A. arenosa [9]. This pattern is diagnostic for tetrasomic inheritance and indicates that A. arenosa has ‘‘cytologically, but not genetically diploidized meiosis’’ [9]. Although A. arenosa is no exception in this respect [4,12], it represents a promising model to understand how this can occur. Yant et al. [10] observed a significant reduction of crossover frequencies in natural autotetraploids compared to diploids and the corresponding colchicine-induced tetraploids. Most bivalents in the natural autotetraploids are held by single chiasmata (see also [13]) whereas a majority of bivalents are bound by at least two chiasmata in diploids and neotetraploids. This result makes much sense, because there is no opportunity for multivalent formation when all chromosomes undergo one (obligatory) crossover only. By contrast, the colchicine-induced tetraploid that ‘grabs too much loses all’ because increased crossover frequencies result in increased meiotic abnormalities. In fact, Yant et al. [10] do far more than just support the longstanding idea that reduced crossover frequency helps to improve chromosome segregation and fertility in autopolyploids. They also shed new
light on, or offer new opportunities to investigate the mechanistic and evolutionary origin of this adaptation. The candidate selected meiotic genes identified in [10] represent a remarkably limited set of functions involved in the early steps of meiotic recombination (AaPRD3, AaASY1, AsASY3, AaZYP1a, AaZYP1b) and sister-chromatid cohesion (AaSYN1, AaSMC6). Owing to its small sample size, this list makes it possible to test whether the selected variants contribute effectively to reduce crossover frequency. The list also raises questions as to why such a specific sample of interrelated genes has been targeted, when meiotic recombination depends on a far wider range of factors. Does this mean that the earliest variant to get selected has set a path that the latter have to follow to keep forging ahead? Or are there preferential targets that one might not see at first glance? In this respect, it is noteworthy that ASY1 has also been hypothesized to contribute to the cytological diploidization of allopolyploid wheat [15]. Notwithstanding this last point, the work of Yant et al. [10] now offers the possibility to test whether the same set of genes has been targeted by natural selection in another cytologically, but not genetically diploidized autopolyploid lineage. One may finally ask whether selection has acted on alleles already segregating within the diploid populations or whether the variants were selected right after they originated in the autotetraploid population(s). The first answer is correct for AaASY1, for which the allele which is almost fixed in the tetraploids
occurs at a very low frequency in the diploids [9]. This result suggests that natural autotetraploid A. arenosa may have originated from the union of parental genotypes fortuitously endowed with beneficial/potentiating mutations already present in the diploid populations. Further investigations are needed to understand whether the same holds true for the other candidate selected meiotic genes and thus how such polygenic architecture has evolved in natural autotetraploid A. arenosa. Despite considerable empirical observations and theoretical predictions, the cytological diploidization of polyploid species has remained a mystery for a long time. The work of Yant et al. [10], together with the molecular characterization of the Ph1 locus in wheat [16], has begun to fill this gap. One would, however, be wrong to believe that reduced chiasma frequency is always a prerequisite for the establishment of a new polyploid species [17–19]. In fact, and as might be expected, hopeful polyploid monsters most likely have more than one trick up their sleeves! References 1. Madlung, A. (2013). Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110, 99–104. 2. Otto, S.P., and Whitton, J. (2000). Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437. 3. Van de Peer, Y., Maere, S., and Meyer, A. (2009). The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10, 725–732. 4. Parisod, C., Holderegger, R., and Brochmann, C. (2010). Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17. 5. Ni, Z., Kim, E.D., Ha, M., Lackey, E., Liu, J., Zhang, Y., Sun, Q., and Chen, Z.J. (2009). Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327–331. 6. Chao, D.Y., Dilkes, B., Luo, H., Douglas, A., Yakubova, E., Lahner, B., and Salt, D.E. (2013). Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341, 658–659. 7. Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100. 8. Albertin, W., and Marullo, P. (2012). Polyploidy in fungi: evolution after whole-genome duplication. Proc. Biol. Sci. 279, 2497–2509. 9. Hollister, J.D., Arnold, B.J., Svedin, E., Xue, K.S., Dilkes, B.P., and Bomblies, K. (2012). Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 8, e1003093. 10. Yant, L., Hollister, J.D., Wright, K.M., Arnold, B.J., Higgins, J.D., Franklin, F.C.H., and Bomblies, K. (2013). Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23, 2151–2156. 11. Grandont, L., Jenczewski, E., and Lloyd, A. (2013). Meiosis and its deviations in polyploid plants. Cytogenet. Genome Res. 140, 171–184.
Dispatch R963
12. Ramsey, J., and Schemske, D.W. (2002). Neopolyploidy in flowering plants. Annu. Rev. Ecol. Systemat. 33, 589–639. 13. Carvalho, A., Delgado, M., Bara˜o, A., Frescatada, M., Ribeiro, E., Pikaard, C., Viegas, W., and Neves, N. (2010). Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa. Sex Plant Reprod. 23, 29–37. 14. Storchova, Z., Breneman, A., Cande, J., Dunn, J., Burbank, K., O’Toole, E., and Pellman, D. (2006). Genome-wide genetic analysis of polyploidy in yeast. Nature 443, 541–547. 15. Boden, S.A., Langridge, P., Spangenberg, G., and Able, J.A. (2009). TaASY1 promotes
homologous chromosome interactions and is affected by deletion of Ph1. Plant J. 57, 487–497. 16. Griffiths, S., Sharp, R., Foote, T.N., Bertin, I., Wanous, M., Reader, S., Colas, I., and Moore, G. (2006). Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439, 749–752. 17. Hazarika, M.H., and Rees, H. (1967). Genotypic control of chromosome behaviour in rye X. Chromosome pairing and fertility in autotetraploids. Heredity 22, 317–332. 18. Crowley, J.G., and Rees, H. (1968). Fertility and selection in tetraploid Lolium. Chromosoma 24, 300–308.
Cell Biology: Cytoskeleton Network Topology Feeds Back on Its Regulation Many cell functions rely on microtubule dynamics and ordering. Two recent studies show that microtubule severing by katanin plays an overbearing role in this process and is primarily regulated at microtubule crossovers. Olivier Hamant By showing how microtubule crossovers are at a central position in the control of cytoskeleton ordering, and by providing a regulatory mechanism underlying this control, the work by Zhang et al. [1] in this issue and Wightman et al. [2] published recently in Current Biology illustrates how plant research provides important new findings that are relevant to cell biology in all kingdoms, with implications in development and biomedical research, too. Understanding the regulation of microtubule dynamics is crucial to many biological processes. This is probably most obvious in plants — in this kingdom, growth is driven by turgor pressure, and the mechanical properties of the cell wall constrain its rate and direction. Because microtubules control the deposition of cellulose [3], and thus the mechanical anisotropy of cell walls, any defect in microtubule behavior is translated into an abnormal macroscopic cell and tissue shape [4]. Most remarkably, when microtubules are depolymerized, aerial plant organs become spherical and cells resemble soap bubbles [5]. Mutants with disorganized microtubules also exhibit isotropic growth, and among the known regulators, the microtubule severing protein katanin has emerged as
one of the main controlling factors. In fact, one of the katanin alleles in Arabidopsis is called botero, referencing the artist’s work reflecting the rather obese and thus isotropic geometry of the corresponding mutant phenotype [6]. Katanin was originally purified in extracts from sea urchin eggs. Since then, this AAA ATPase has been found in all eukaryotes and acts as an heterodimer, with the 60 kDa katanin subunit displaying the catalytic activity, and the 80 kDa WD40-repeat counterpart displaying a regulatory role [7]. Importantly, while the function of katanin was initially associated with centrosomal microtubules, there is now evidence that this role is also relevant to non-centrosomal microtubules. This is not only illustrated by the work conducted in plants — katanin is also involved in the control of axonal growth [8] and cell migration [9]. Katanin has also been proposed to increase the number of short microtubule fragments near meiotic chromatin to compensate for their rather inefficient nucleation in this context [10]. Therefore, the work that is highlighted here [1,2] consolidates some ideas and provides a number of predictions that may change the way we understand microtubule ordering in all eukaryotes. Briefly, Zhang et al. [1] show that katanin activity is triggered through
19. Brubaker, C.L., Paterson, A.H., and Wendel, J.F. (1999). Comparative genetic mapping of allotetraploid cotton and its diploid progenitors. Genome 42, 184–203.
1INRA, UMR1318, Institut Jean-Pierre Bourgin, RD10, F-78000 Versailles, France. 2AgroParisTech, Institut Jean-Pierre Bourgin, RD10, F-78000 Versailles, France. E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2013.09.023
one dominant mechanism: cutting microtubules where they cross each other. Microtubule severing had previously been shown to occur preferentially at microtubule crossovers in a seminal article [11]. The work by Zhang et al. thus narrows down the molecular mechanism to only one predominant factor — katanin. In particular, they show that this enzyme localizes to microtubule crossovers and that in a katanin mutant, severing at crossovers is completely absent (Figure 1). Interestingly, a quantitative analysis of the corresponding kinetics highlights that longer-lived crossovers are more prone to severing than early ones, demonstrating that microtubule crossovers act both as a spatial and temporal regulator of severing [1]. This provides a feedback loop in which microtubule severing by katanin promotes the organization of the microtubule network, which in turn, through the amount, position and age of crossovers, regulates katanin activity. Because of their prevailing role in controlling microtubule organization, crossovers in the microtubule network emerge as a central regulatory point in plant cell biology. The work by Wightman, et al. [2] illustrates this idea by providing a new regulatory module that relies on microtubule crossovers. The authors notably show that the presence of highly aligned microtubule bundles in the spiral2 mutant is due to the inhibition of severing by SPR2, a previously identified microtubule-associated protein (MAP). More strikingly, they found that SPR2 accumulates at microtubule crossovers, where it prevents severing locally (Figure 1). Interestingly, this activity is also modulated in different cell types — the increased severing