期刊论文详细信息
BMC Developmental Biology
Expression of pair rule gene orthologs in the blastoderm of a myriapod: evidence for pair rule-like mechanisms?
Graham E Budd2  Wim G M Damen1  Ralf Janssen2 
[1] Department of Genetics, Friedrich-Schiller-University Jena, Philosophenweg 12, 07743, Jena, Germany;Department of Earth Sciences, Uppsala University, Villavägen 16, 752 36, Uppsala, Sweden
关键词: Odd-skipped;    Sloppy-paired;    Odd-paired;    Hairy;    Runt;    Even-skipped;    Paired;    Segmentation;    Pair rule patterning;    Evolution;   
Others  :  1086629
DOI  :  10.1186/1471-213X-12-15
 received in 2011-10-17, accepted in 2012-04-11,  发布年份 2012
PDF
【 摘 要 】

Background

A hallmark of Drosophila segmentation is the stepwise subdivision of the body into smaller and smaller units, and finally into the segments. This is achieved by the function of the well-understood segmentation gene cascade. The first molecular sign of a segmented body appears with the action of the pair rule genes, which are expressed as transversal stripes in alternating segments. Drosophila development, however, is derived, and in most other arthropods only the anterior body is patterned (almost) simultaneously from a pre-existing field of cells; posterior segments are added sequentially from a posterior segment addition zone. A long-standing question is to what extent segmentation mechanisms known from Drosophila may be conserved in short-germ arthropods. Despite the derived developmental modes, it appears more likely that conserved mechanisms can be found in anterior patterning.

Results

Expression analysis of pair rule gene orthologs in the blastoderm of the pill millipede Glomeris marginata (Myriapoda: Diplopoda) suggests that these genes are generally involved in segmenting the anterior embryo. We find that the Glomeris pairberry-1 ( pby-1) gene is expressed in a pair rule pattern that is also found in insects and a chelicerate, the mite Tetraynchus urticae. Other Glomeris pair rule gene orthologs are expressed in double segment wide domains in the blastoderm, which at subsequent stages split into two stripes in adjacent segments.

Conclusions

The expression patterns of the millipede pair rule gene orthologs resemble pair rule patterning in Drosophila and other insects, and thus represent evidence for the presence of an ancestral pair rule-like mechanism in myriapods. We discuss the possibilities that blastoderm patterning may be conserved in long-germ and short-germ arthropods, and that a posterior double segmental mechanism may be present in short-germ arthropods.

【 授权许可】

   
2012 Janssen et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150116013608274.pdf 3215KB PDF download
Figure 9. 46KB Image download
Figure 8. 46KB Image download
Figure 7. 47KB Image download
Figure 6. 74KB Image download
Figure 5. 33KB Image download
Figure 4. 107KB Image download
Figure 3. 76KB Image download
Figure 2. 49KB Image download
Figure 1. 196KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】
  • [1]Akam M: The molecular basis for metameric pattern in the Drosophila embryo. Development 1987, 101:1-22.
  • [2]Pankratz MJ, Jäckle H: Blastoderm segmentation. In The development of Drosophila melanogaster. Edited by Bate M, Martinez Arias A. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1993:467-516.
  • [3]Davis GK, Patel NH: Playing by pair rules? BioEssays 2003, 25:425-429.
  • [4]Fröhnhofer HG, Nüsslein-Volhard C: Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 1986, 324:120-125.
  • [5]McGregor AP: How to get ahead: the origin, evolution and function of bicoid. BioEssays 2005, 27:904-913.
  • [6]Jäckle H, Hoch M, Pankratz MJ, Gerwin N, Sauer F, Brönner G: Transcriptional control by Drosophila gap genes. J Cell Sci Suppl 1992, 16:39-51.
  • [7]Ingham PW, Baker NE, Martinez-Arias A: Regulation of segment polarity genes in the Drosophila blastoderm by fushi tarazu and even skipped. Nature 1988, 331:73-75.
  • [8]Cadigan KM, Grossniklaus U, Gehring WJ: Localized expression of sloppy paired protein maintains the polarity of Drosophila parasegments. Genes Dev 1994, 8:899-913.
  • [9]Sanson B: Generating patterns from fields of cells. EMBO reports 2001, 2:1083-1088.
  • [10]Davis GK, Patel NH: Short, long and beyond: molecular and embryological approaches to insect segmentation. Annu Rev Entomol 2002, 47:669-699.
  • [11]Janssen R, Prpic NM, Damen WG: Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 2004, 268:89-104.
  • [12]Janssen R, Budd GE, Damen WG, Prpic NM: Evidence for Wg-independent tergite boundary formation in the millipede Glomeris marginata. Dev Genes Evol 2008, 218:361-370.
  • [13]Damen WG: Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 2002, 129:1239-1250.
  • [14]Hughes CL, Kaufman TC: Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev Biol 2002, 247:47-61.
  • [15]Hughes CL, Kaufman TC: Hox genes and the evolution of the arthropod body plan. Evol Dev 2002, 4:459-499.
  • [16]Eriksson BJ, Tait NN, Budd GE, Akam M: The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996). Dev Genes Evol 2009, 219:249-264.
  • [17]Eriksson BJ, Tait NN, Budd GE, Janssen R, Akam M: Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev Genes Evol 2010, 220:117-122.
  • [18]Damen WG: Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 2007, 236:1379-1391.
  • [19]Aranda M, Marques-Souza H, Bayer T, Tautz D: The role of the segmentation gene hairy in Tribolium. Dev Genes Evol 2008, 218:465-477.
  • [20]Choe CP, Miller SC, Brown SJ: A pair rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc Natl Acad Sci USA 2006, 103:6560-6564.
  • [21]Erezyilmaz DF, Kestrup HC, Riddiford LM: The nuclear receptor E75E has a novel pair-rule-like function in patterning the milkweed bug, Oncopeltus fasciatus. Dev Biol 2009, 334:300-310.
  • [22]Binner P, Sander K: Pair-rule patterning in the honeybee Apis mellifera: Expression of even-skipped combines traits known from beetles and fruitfly. Dev Genes Evol 1997, 206:447-454.
  • [23]Wilson MJ, Havler M, Dearden PK: Giant, Krüppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo. Dev Biol 2010, 339:200-211.
  • [24]Janssen R, Budd GE, Prpic NM, Damen WG: Expression of myriapod pair rule gene orthologs. Evodevo 2011, 2:5. BioMed Central Full Text
  • [25]Damen WG, Janssen R, Prpic NM: Pair rule gene orthologs in spider segmentation. Evol Dev 2005, 7:618-628.
  • [26]Schoppmeier M, Damen WG: Expression of Pax group III genes suggests a single-segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei. Evol Dev 2005, 7:160-167.
  • [27]Brown SJ, Parrish JK, Beeman RW, Denell RE: Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum. Mech Dev 1997, 61:165-173.
  • [28]Mito T, Kobayashi C, Sarshima I, Hongjie Z, Shinahara W, Miyawaki K, Shinmyo Y, Ohuchi H, Noji S: Even-skipped has gap-like, pair-rule-like, and segmental functions in the cricket Gryllus bimaculatus, a basal, intermediate germ insect (Orthoptera). Dev Biol 2007, 303:202-213.
  • [29]Peel A: The evolution of arthropod segmentation mechanisms. BioEssays 2004, 26:1108-1111.
  • [30]Dearden PK, Donly C, Grbic M: Expression of pair rule gene homologues: early patterning of the two-spotted spider mite Tetranychus urticae. Development 2002, 129:5461-5472.
  • [31]Pechmann M, McGregor AP, Schwager EE, Feitosa NM, Damen WG: Dynamic gene expression is required for anterior regionalization in a spider. Proc Natl Acad Sci USA 2009, 106:1468-1472.
  • [32]Janssen R, Damen WG: The ten Hox genes of the millipede Glomeris marginata. Dev Genes Evol 2006, 216:451-465.
  • [33]Telford MJ: Evidence for the derivation of the Drosophila fushi tarazu gene from a Hox gene orthologous to lophotrochozoan Lox5. Curr Biol 2000, 10:349-352.
  • [34]Damen WG: Fushi tarazu: a Hox gene changes its role. Bioessays 2002, 24:992-995.
  • [35]Prpic NM, Tautz D: The expression of the proximodistal axis patterning genes Distal-less and dachshund in the appendages of Glomeris marginata (Myriapoda: Diplopoda) suggests a special role of these genes in patterning the head appendages. Dev Biol 2003, 260:97-112.
  • [36]Dohle W: Die Embryonalentwicklung von Glomeris marginata (Villers) im Vergleich zur Entwicklung anderer Diplopoden. Zool Jahrb Anat 1964, 81:241-310.
  • [37]Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE, Brown SJ, Prpic NM, Kosiol C, Damen WG, Balavoine G, McGregor AP: Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of axis elongation and segmentation. BMC Evol Biol 2010, 10:374. BioMed Central Full Text
  • [38]Goto T, Macdonald P, Maniatis T: Early and late periodic patterns of even skipped expression are controlled by distinct regulatory elements that respond to different spatial cues. Cell 1989, 57:413-422.
  • [39]Small S, Blair A, Levine M: Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J 1992, 11:4047-4057.
  • [40]Small S, Arnosti DN, Levine M: Spacing ensures autonomous expression of different stripe enhancers in the even-skipped promoter. Development 1993, 119:762-772.
  • [41]Fujioka M, Jaynes JB, Goto T: Early even-skipped stripes act as morphogenetic gradients at the single cell level to establish engrailed expression. Development 1995, 121:4371-4382.
  • [42]Schroeder R, Jay DG, Tautz D: Elimination of EVE protein by CALI in the short germ band insect Tribolium suggests a conserved pair-rule function for even skipped. Mech Dev 1999, 80:191-195.
  • [43]Liu PZ, Kaufman TC: even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect. Development 2005, 132:2081-2092.
  • [44]Janssen R: Diplosegmentation in the pill millipede Glomeris marginata is the result of dorsal fusion. Evol Dev 2011, 13:477-487.
  • [45]Janssen R, Damen WG, Budd GE: Expression of collier in the premandibular segment of myriapods: support for the traditional Atelocerata concept or a case of convergence? BMC Evol Biol 2011, 11:50. BioMed Central Full Text
  • [46]Schroeder MD, Greer C, Gaul U: How to make stripes: deciphering the transition from non-periodic to periodic patterns in Drosophila segmentation. Development 2011, 138:3067-3078.
  • [47]Langeland JA, Carroll SB: Conservation of regulatory elements controlling hairy pair-rule stripe formation. Development 1993, 117:585-596.
  • [48]Pueyo JI, Lanfear R, Couso JP: Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana. Proc Natl Acad Sci USA 2008, 105:16614-16619.
  • [49]Grossniklaus U, Cadigan KM, Gehring WJ: Three maternal coordinate systems cooperate in the patterning of the Drosophila head. Development 1994, 120:3155-3171.
  • [50]Baumgartner S, Noll M: Network of interactions among pair-rule genes regulating paired expression during primordial segmentation of Drosophila. Mech Dev 1990, 33:1-18.
  • [51]Choe CP, Brown SJF: Evolutionary flexibility of pair rule patterning revealed by functional analysis of secondary pair rule genes, paired and sloppy-paired in the short-germ insect, Tribolium castaneum. Dev Biol 2007, 302:281-294.
  • [52]Osborne PW, Dearden PK: Expression of Pax group III genes in the honeybee (Apis mellifera). Dev Genes Evol 2005, 215:499-508.
  • [53]Davis GK, Jaramillo CA, Patel NH: Pax Group III genes and the evolution of insect pair rule patterning. Development 2001, 128:3445-3458.
  • [54]Benedyk MJ, Mullen JR, DiNardo S: odd-paired: a zinc finger pair rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev 1994, 8:105-117.
  • [55]Chipman AD, Arthur W, Akam M: A double segment periodicity underlies segment generation in centipede development. Curr Biol 2004, 14:1250-1255.
  • [56]Gutjahr T, Frei E, Noll MF: Complex regulation of early paired expression: initial activation by gap genes and pattern modulation by pair rule genes. Development 1993, 117:609-623.
  • [57]Keller RG, Desplan C, Rosenberg MI: Identification and characterization of Nasonia Pax genes. Ins Mol Biol 2010, 19:109-120.
  • [58]Mittmann B, Scholtz G: Development of the nervous system in the “head” of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev Genes Evol 2003, 213:9-17.
  • [59]Harzsch S, Wildt M, Battelle B, Waloszek D: Immunohistochemical localization of neurotransmitters in the nervous system of larval Limulus polyphemus (Chelicerata, Xiphosura): evidence for a conserved protocerebral architecture in Euarthropoda. Arthropod Struct Dev 2005, 34:327-342.
  • [60]Telford MJ, Thomas RH: Expression of homeobox genes shows chelicerate arthropods retain their deuterocerebral segment. Proc Natl Acad Sci USA 1998, 95:10671-10675.
  • [61]Damen WG, Hausdorf M, Seyfarth E-A, Tautz D: A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 1998, 95:10665-10670.
  • [62]Goltsev Y, Hsiong W, Lanzaro G, Levine M: Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev Biol 2004, 275:435-446.
  • [63]Eckert C, Aranda M, Wolff C, Tautz D: Separable stripe enhancer elements for the pair rule gene hairy in the beetle Tribolium. EMBO Rep 2004, 5:638-642.
  • [64]Mito T, Okamoto H, Shinahara W, Shinmyo Y, Miyawaki K, Ohuchi H, Noji S: Krüppel acts as a gap gene regulating expression of hunchback and even-skipped in the intermediate germ cricket Gryllus bimaculatus. Dev Biol 2006, 294:471-481.
  • [65]García-Solache M, Jaeger J, Akam M: A systematic analysis of the gap gene system in the moth midge Clogmia albipunctata. Dev Biol 2010, 344:306-318.
  • [66]Sander K: Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol 1976, 12:125-238.
  • [67]Damen WG, Weller M, Tautz D: The expression patterns of hairy, even-skipped, and runt in the spider Cupiennius salei imply that these genes were segmentation genes in a basal arthropod. Proc Natl Acad Sci USA 2000, 97:4515-4519.
  • [68]Chipman AD, Akam M: The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pair rule gene homologues. Dev Biol 2008, 319:160-169.
  • [69]Macdonald PM, Ingham P, Struhl G: Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell 1986, 47:721-734.
  • [70]Janssen R, Budd GE, Damen WG: Gene expression suggests conserved mechanisms patterning the heads of insects and myriapods. Dev Biol 2011, 357:64-72.
  • [71]Peel A, Akam M: Evolution of segmentation: Rolling back the clock. Curr Biol 2003, 13:R708-R710.
  • [72]Arthur W, Chipman AD: The centipede Strigamia maritima: what it can tell us about the development and evolution of segmentation. BioEssays 2005, 27:653-660.
  • [73]Edgecombe GD, Giribet G: Evolutionary biology of centipedes (Myriapoda: Chilopoda). Annu Rev Entomol 2007, 52:151-170.
  • [74]Arthur W, Farrow M: The pattern of variation in centipede segment number as an example of developmental constraint in evolution. J Theor Biol 1999, 200:183-191.
  文献评价指标  
  下载次数:1次 浏览次数:10次