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provided by Elsevier - Publisher Connector Current Biology Vol 20 No 23 R1020

example, the bulk of the genome has for future studies. Immediate questions Biology of the Cell, Fourth Edition, (New York & Abingdon: Garland Science). replicated by about 15 minutes into S14 that come to mind are: What is the 2. Shermoen, A.W., McCleland, M.L., and whereas satellite DNA sequences schedule of appearance of other O’Farrell, P.H. (2010). Developmental control of bEGAN incorporating nucleotide markers of heterochromatin, such as late replication and S phase length. Curr. Biol. 20, 2067–2077. analogs only after bulk DNA has histone modifications and Sir proteins? 3. Foe, V.E., Odell, G.M., and Edgar, B.A. (1993). stopped incorporating nucleotide Do checkpoint functions encoded by Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In The analogs. Different classes of satellite grapes and mei-41 have a role in Development of Drosophila melanogaster, DNA, which differ by the sequence delaying mitosis, i.e. lengthening Volume 1, M. Bates and A.M. Arias, eds. (Cold repeated, follow different schedules. interphase, when satellite DNA Spring harbor: CSH Laboratory Press), pp. 149–300. Generally speaking, each block takes becomes late-replicating? Do DNA 4. McCleland, M.L., Shermoen, A.W., and about 10 minutes to replicate such that checkpoints themselves act to delay O’Farrell, P.H. (2009). DNA replication times the cell cycle and contributes to the mid-blastula S14 lasts about 50 minutes in total. the replication of satellite DNA, as they transition in Drosophila embryos. J. Cell Biol. These results are at odds with the act to delay DNA synthesis when the 187, 7–14. model that titration of maternal factor genome is damaged? When reduction 5. Sibon, O.C., Laurencon, A., Hawley, R., and Theurkauf, W.E. (1999). The Drosophila ATM (s) lengthen S phase. Instead, the of cyclins rescues mei-41-depleted homologue Mei-41 has an essential checkpoint results are more consistent with an embryos without restoring interphase function at the midblastula transition. Curr. Biol. 9, 302–312. active delaying of satellite DNA length [5], what happens to the 6. Fogarty, P., Campbell, S.D., Abu-Shumays, R., replication. In support of this idea, temporal order of replication? Perhaps Phalle, B.S., Yu, K.R., Uy, G.L., Goldberg, M.L., blocking zygotic transcription with a- the most intriguing question concerns and Sullivan, W. (1997). The Drosophila grapes gene is related to checkpoint gene chk1/rad27 amanatin, an inhibitor of RNA the developmental signal that is and is required for late syncytial division polymerases, ‘blocked’ late replication; dependent on zygotic transcription and fidelity. Curr. Biol. 7, 418–426. 7. Shermoen, A.W., and O’Farrell, P.H. (1991). under these conditions, satellite DNAs is responsible for the lengthening of the Progression of the cell cycle through mitosis replicated with bulk DNA. S phase. What is it, how does it direct leads to abortion of nascent transcripts. Cell The findings by Shermoen and the timing of replication of satellite 67, 303–310. 8. Grosshans, J., and Wieschaus, E. (2000). A colleagues [2] lead to several important sequences and why is its effect more genetic link between morphogenesis and cell new insights listed here. severe for some sequences than division during formation of the ventral furrow in Drosophila. Cell 101, 523–531. Heterochromatin formation as defined others? Finally, how applicable are 9. Mata, J., Curado, S., Ephrussi, A., and Rorth, P. by HP1 binding follows rather than findings in Drosophila embryos to (2000). Tribbles coordinates mitosis and proceeds late replication. Late embryos of other systems? During morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101, 511–522. replication is not uniform but involves mouse embryogenesis, genomic 10. Seher, T.C., and Leptin, M. (2000). Tribbles, discrete satellite sequences replicating domains adopt different replication a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila in a defined temporal sequence after schedules in concert with loss of gastrulation. Curr. Biol. 10, 623–629. the completion of bulk DNA replication. pluripotency or cell fate commitment 11. Pope, B.D., Hiratani, I., and Gilbert, D.M. (2010). Finally, lengthening of S phase is [11]. It would be worthwhile to Domain-wide regulation of DNA replication timing during mammalian development. a result of a development transition, investigate if developmental cues that Chromosome Res. 18, 127–136. likely driven by zygotic transcription, direct the replication timing of satellite in which satellite sequences become DNA in Drosophila embryos also act on Molecular, Cellular and Developmental late replicating. mammalian genomic regions during Biology, 347 UCB, University of Colorado, Interphase lengthening that is differentiation. Boulder, CO 80309-0347, USA. brought about by late replication of E-mail: [email protected] satellite DNA may serve a purpose. References Longer interphases would allow for 1. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., and Walter, P. (2002). Molecular DOI: 10.1016/j.cub.2010.11.003 complete transcription of long genes. The transcription unit for Ubx, for example, is 77 kb long and RNA polymerase would require approximately 55 minutes to transverse it from end to end. In fact, Pollination: Sexual Abounds nascent Ubx transcripts are aborted upon mitosis in cycles with short interphases and become complete only Why do plants mimic female to attract males for pollination? A new in cycles with longer interphases [7]. study gives insights into the advantages of and documents this Secondly, because cytoskeletal pollination system for the first time outside the orchid family, in a South African arrangements for mitosis and cell daisy. motility are incompatible, longer interphases may be necessary to allow cell movements that constitute Florian P. Schiestl speculum, with their shiny blue gastrulation. Indeed, premature entry center and dark-red margin of long into M14, i.e.? shortening interphase Animal-like flowers have always hairs, were interpreted for the first time 14 experimentally, disrupts fascinated botanists, but the adaptive as imitating female insects to attract gastrulation in Drosophila embryos value of such resemblance remained males for pollination [1]. Soon after, [8–10]. undiscovered for a long time. It was not such sexual mimicry was found in an The work by Shermoen and until the beginning of the 20th century Australian orchid [2]. At the time, these colleagues [2] also provides questions that flowers of the terrestrial orchid interpretations were met with disbelief, Dispatch R1021 and were only proven true some 40 years later in detailed experimental investigations [3]. Since then, pollination by ‘sexual deception’ has been investigated in detail and is now considerably well understood. Sexually deceptive flowers usually do not produce any reward for their but mimic certain key signals of their pollinators’ mating behavior; the pollinators, exclusively male insects, transfer the pollen during mating attempts, so-called ‘pseudocopulations’ [4]. Although new sexually deceptive pollination systems are continuously being discovered among orchids [5], the recent first experimental proof of pollination by pseudocopulation outside the deserves special attention. In a recent issue of The American Naturalist, Ellis and Johnson [6] report pollination by sexual Figure 1. An inflorescence of Gorteria diffusa, representing the sexually deceptive ‘Spring’ deception in the South African daisy morphotype. Gorteria diffusa. With several earlier The inflorescence is visited by the bombyliid fly, Megapalpus capensis, covered in pollen. reports of -like flowers in this and (photo courtesy of S. Johnson.) other non-orchid taxa [7,8], this discovery was perhaps anticipated, yet surprising at the same time. systems. Orchids often exploit male One of the most striking features of Sexual deception is a highly as pollinators, which Gorteria diffusa is its extreme floral specialized, deceptive pollination learn to avoid individual flowers, variability, which evolved without mechanism which relies on the one or locations with flowers, after corresponding switches in pollinators, hand on pre-adaptations enabling pseudocopulation [12,13]. This as all allopatric Gorteria forms share mimicry of the body and mating signals avoidance learning contributes to the same species [14]. of a pollinator [9], and on the other hand the overall low visitation rate typically The new study now shows that this on a highly efficient pollination system, observed in these orchids; however, variation, instead, is linked to different because pollinator visitation frequency even infrequent pollinator visits can degrees of sexual mimicry, and thus is typically low [10]. Daisies such as lead to fertilization of many ovules different responses by the pollinators, Gorteria are characterized by floral due to the orchids’ highly efficient ranging from food-seeking behavior in traits that are traditionally considered pollination system. Moreover, both sexes to full pseudocopulation to constrain the evolution of pollination with pollinia makes displayed only by males. This unique specialized pollination systems, such avoidance learning a key feature for situation provides ideal opportunities as granular pollen and single ovules per outcrossing, because pollinia-carrying to investigate the evolution of floral flower, nectar production in shallow pollinators that return to an individual traits involved in sexual mimicry, as flowers, as well as radially symmetric, flower can cause massive self well as the evolutionary forces leading colorful inflorescences. In contrast, pollination. The lack of avoidance to such unusual exploitation of orchid pollen is typically packed learning in male bombyliid pollinators pollinators. Ellis and Johnson [6] used together into pollinia, and flowers of Gorteria, in contrast, seems to be fluorescent powder as a pollen produce many ovules, making almost a prerequisite for sexual analogue, and showed that pollination pollination highly efficient. Sexually deception in a pollination system with by pseudocopulating males leads deceptive orchid species produce granular pollen, which lacks the high to higher pollen export compared no nectar and mimic an insect body efficiency of orchid pollinia. But why to food-reward based pollination. through one modified , the do male flies not learn to avoid flower Male flies showed higher activity labellum. Gorteria employs a different mimics? Male flies may simply be than females, with shorter but more strategy, as it mimics insects sitting unable to learn individual floral traits frequent visitations to flowers, and on the inflorescence by producing due to memory constraints, or may not more movements between plants. elevated dark spots on orange be selected for avoidance learning Interestingly, similar results were found in non-symmetrical arrays (Figure 1), because of a polyandrous mating earlier for foraging solitary , where the development of which is now well system, with females mating multiple males made shorter visits and foraged understood [11]. Interestingly, the times. Overall, the Gorteria example in more distant patches than females pollinators of Gorteria, male bombyliid is a telling story about the behavior of [15]. In Mediterranean sexually flies (Figure 1), attempt to copulate with a pollinator playing a crucial role for its deceptive orchids, pollinated by floral spots frequently [6], which differs suitability in a specialized pollination male solitary bees, a higher efficiency from sexually deceptive orchid system. of pollen export compared to Current Biology Vol 20 No 23 R1022 food-deceptive orchids pollinated becoming more commonly known 9. Schiestl, F.P., and Cozzolino, S. (2008). Evolution of sexual mimicry in the orchid primarily by female bees, has also been [16–18], and the evolutionary subtribe orchidinae: the role of preadaptations shown recently [10]. Collectively, these mechanisms through pre-existing bias in the attraction of male bees as pollinators. data suggest that specificity and better understood [19,20]. The new BMC Evol. Biol. 8, 27. 10. Scopece, G., Cozzolino, S., Johnson, S.D., and exploitation of male mating behavior study by Ellis and Johnson highlights Schiestl, F.P. (2010). Pollination efficiency and provide higher male fitness for the that pollination through male mating the evolution of specialized deceptive pollination systems. Am. Nat. 175, 98–105. plants through improved pollen export. behavior can convey selective 11. Thomas, M.M., Rudall, P.J., Ellis, A.G., Within Gorteria, some forms advantages and, further, that Savolainen, V., and Glover, B.J. (2009). nevertheless rely mostly on pollination prerequisites of sexual floral mimicry Development of a complex floral trait: the pollinator-attracting petal spots of the by food-seeking females, perhaps are not limited to orchids. daisy, Gorteria diffusa (Asteraceae). Am. J. Bot. because it optimizes pollination Nevertheless, orchids have evolved 96, 2184–2196. 12. Ayasse, M., Schiestl, F.P., Paulus, H.F., success, the female component of the most sophisticated examples of Lofstedt, C., Hansson, B., Ibarra, F., and reproductive fitness [6]. female-insect imitations, some being Francke, W. (2000). Evolution of reproductive In Gorteria, pseudocopulation striking even to human eyes. But strategies in the sexually deceptive orchid Ophrys sphegodes: How does flower-specific obviously evolved from food reward. besides these textbook examples of variation of odor signals influence reproductive In some forms, perhaps representing sexual deception, a sharpened focus success? Evolution 54, 1995–2006. 13. Peakall, R. (1990). Responses of male the intermediate evolutionary stage, will likely unravel more subtle forms Zaspilothynnus trilobatus Turner to simple petal spots only release of sexual mimicry in various plant females and the sexually deceptive orchid it inspecting-behavior by male insects, taxa in the future. pollinates. Func. Ecol. 4, 159–167. 14. Ellis, A.G., and Johnson, S.D. (2009). The but no pseudocopulation [6]. evolution of floral variation without pollinator Spots eliciting pseudocopulations are shifts in Gorteria diffusa (Asteraceae). Am. J. References Bot. 96, 793–801. three-dimensional ornaments 1. Pouyanne, A. (1917). Le fecondation des 15. Ne’eman, G., Shavit, O., Shaltiel, L., and consisting of three types of specialized Ophrys par les insectes. Bull. Soc. Hist. Nat. Shmida, A. (2006). Foraging by male and female cells [11], with possible scent emission Afr. Nord. 8, 6–7. solitary bees with implications for pollination. J. 2. Coleman, E. (1927). Pollination of the orchid Insect Behav. 19, 383–401. not yet investigated. The selective leptochila. Victorian Naturalist 44, 16. Vereecken, N.J., and Schiestl, F.P. (2008). force leading to a continuous 20–22. The evolution of imperfect floral mimicry. Proc. 3. Kullenberg, B. (1961). Studies in Ophrys Natl. Acad. Sci. USA 105, 7484–7488. elaboration of petal spots is likely the Pollination, Volume 34 (Uppsala: Zool. Bidrag), 17. Van Kleunen, M., Nanni, I., Donaldson, J.S., and pre-existing preference of males for pp. 1–340. Manning, J.C. (2007). The role of beetle marks female-like features. Sexual deception 4. Schiestl, F.P. (2005). On the success of and flower colour on visitation by monkey a swindle: pollination by deception in orchids. (Hopliini) in the greater cape floral thus evolves under pre-existing bias Naturwissenschaften 92, 255–264. region, South Africa. Ann. Bot. 100, 1483–1489. of male pollinators selecting for 5. Ciotek, L., Giorgis, P., Benitez-Vieyra, S., and 18. Biesmeijer, J.C., Giurfa, M., Koedam, D., Cocucci, A.A. (2006). First confirmed case Potts, S.G., Joel, D.M., and Dafni, A. (2005). different degrees of floral mimicry. of pseudocopulation in terrestrial orchids of Convergent evolution: floral guides, stingless As shown by Ellis and Johnson [6], South America: pollination of Geoblasta nest entrances, and insectivorous pitchers. Gorteria forms eliciting mating pennicillata (Orchidaceae) by Campsomeris Naturwissenschaften 92, 444–450. bistrimacula (Hymenoptera, ). Flora 19. 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Male Meiosis: Y Keep It Silenced? DNA double-strand breaks (DSBs), which are repaired through recombination between the What drives defective spermatocytes into apoptosis during mid-pachytene? homologues. This happens within a A recent study identifies the first mid-pachytene ‘killer’ genes: two Y-linked prominent meiosis-specific chromatin transcription factors, the Zfy1/2 gene pair, must be silenced to avoid apoptosis. structure, the synaptonemal complex (SC; reviewed in [1–5]). To prevent formation of gametes with Attila To´ th and Rolf Jessberger chromosomes (homologues, i.e. two abnormal genomic content, pairs of sister chromatids) during gametogenesis must be blocked in Successful reductional meiotic division the first meiotic prophase in most spermatocytes that fail to form COs and the generation of haploid gametes organisms, including mammals. between all pairs of homologues and/or requires the formation of crossovers Inter-homologue CO formation fail to repair DSBs. Indeed, for many (COs) between homologous involves the active generation of decades researchers have noted that