From simplicity to complexity: The gain or loss of spot rows underlies the morphological diversity of threeDrosophilaspecies

Dion, William; Shittu, Mujeeb; Steenwinkel, Tessa E.; Raja, Komal Kumar Bollepogu; Kokate, Prajakta; Werner, Thomas

doi:10.1101/2020.04.03.024778

Cited by 2 publications

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“…wg, dpp , and hh are homologous to known proto-oncogenes in humans 24 , while zen and abdA are Hox genes. The abdominal color pattern of D. guttifera appears to be regulated by multiple developmental pathways consisting of activators and repressors acting in parallel, possibly targeting pigmentation genes other than y as well 18,19,25,26 . Further evidence for the repression of stripes can be seen in Drosophila falleni ’s intraspecific pigment variation, another member of the quinaria species group (Extended Data Fig.…”

Section: Figurementioning

confidence: 99%

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

Raja

Shittu

Nouhan

et al. 2020

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23Changes in cis-regulatory modules (CRMs) that control developmental gene expression 24 patterns have been implicated in the evolution of animal morphology 1-6 . However, the 25 genetic mechanisms underlying complex morphological traits remain largely unknown. 26 Here we investigated the molecular mechanisms that induce the pigmentation gene yellow 27 (y) in a complex spot and shade pattern on the abdomen of the quinaria group species 28 Drosophila guttifera. We show that the y expression pattern is controlled by only one CRM, 29 which contains a stripe-inducing CRM at its core. We identified several developmental 30 genes that may collectively interact with the CRM to orchestrate the patterning in the 31 pupal abdomen of D. guttifera. We further show that the core CRM is conserved among D. 32 guttifera and the closely related quinaria group species Drosophila deflecta, which displays 33 a similarly spotted abdominal pigment pattern. Our data suggest that besides direct 34 activation of patterns in distinct spots, abdominal spot patterns in Drosophila species may 35 have evolved through partial repression of an ancestral stripe pattern, leaving isolated 36 spots behind. Abdominal pigment patterns of extant quinaria group species support the 37 partial repression hypothesis and further emphasize the modularity of the D. guttifera 38 pattern. 39 40 How complex morphological features develop and evolve is a question of foremost importance 41 in biology. To address this question, we identified genes underlying abdominal pigmentation 42 pattern development in Drosophila guttifera (D. guttifera). The abdomen is decorated with six 43 rows of black spots that run along the anterior-posterior axis, divided by a dark dorsal midline 44shade. This color pattern shows four sub-patterns: a dorsal, median, and lateral pair of spot rows, 45 plus the dorsal midline shade (Fig. 1a, b). D. guttifera belongs to the quinaria species group, 46 whose members display highly diverse abdominal pigmentation patterns 7,8 . While D. guttifera 47 dorsal midline (Extended Data Fig. 2c). Similarly, wg foreshadowed all six rows of spots, while 126 dpp expression matched all but the lateral spot rows (Extended Data Fig. 3b, c). In contrast to the 127 D. guttifera results, abd-A, hh, and zen were absent along the dorsal midline, which is in 128 agreement with the lack of pigment in D. deflecta adults (Extended Data Fig. 3d, e, f, g). 129However, abd-A expression was not detectable where the lateral spot rows will form (Extended 130 Data Fig. 3d), suggesting that these particular spots are controlled differently in D. deflecta. We 131 next cloned the 938 bp orthologous def y spot CRM and transformed it into D. guttifera, using 132 the DsRed reporter assay. The def y spot CRM drove faint dorsal spot row and stripe expression, 133 especially along the dorsal spots (Extended Data Fig. 4). We further subdivided the def y spot 134 CRM into 8 sub-fragments and identified a minimal def y core stripe CRM (288 bp) (#7, 135 Extended Data Fig. 4). This...

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Section: Figurementioning

confidence: 99%

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

Raja

Shittu

Nouhan

et al. 2020

Preprint

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“…These studies suggest that t is an important player in the evolution of morphological diversity in Drosophila species. Most interestingly, t expression has co-evolved with y expression [22,23], where both genes are co-expressed in the developing adult cuticle of diverse Drosophila species [33]. Although these two genes have been known to be co-expressed over considerable evolutionary time [22,27], very few studies have demonstrated how two or more genes are transcriptionally coupled and regulated.…”

Section: Introductionmentioning

confidence: 99%

The Genetic Mechanisms Underlying the Concerted Expression of the Yellow and Tan Genes in Complex Patterns on the Abdomen and Wings of Drosophila Guttifera

Raja¹,

Bachman²,

Fernholz³

et al. 2022

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How complex morphological patterns form is an intriguing question in developmental biology. However, the mechanisms that generate complex patterns remain largely unknown. Here we sought to identify the genetic mechanisms that regulate the tan (t) gene in a multi-spotted pigmentation pattern on the abdomen and wings of Drosophila guttifera. Previously, we showed that yellow (y) gene expression completely prefigures the abdominal [1] and wing [2] pigment patterns of this species. In the current study, we demonstrate that the t gene is co-expressed with the y gene in nearly identical patterns, both transcripts foreshadowing the adult abdominal and wing melanin spot patterns. We identified cis-regulatory modules (CRMs) of t, one of which drives reporter expression in six longitudinal rows of spots on the developing pupal abdomen, while the second CRM activates the reporter gene in a spotted wing pattern. Comparing the abdominal spot CRMs of y and t, we found a similar composition of putative transcription factor binding sites that are thought to regulate the complex expression patterns of both terminal pigmentation genes y and t. In contrast, the y and t wing spots appear to be regulated by distinct upstream factors. Our results suggest that the D. guttifera abdominal and wing melanin spot patterns have been established through the co-regulation of y and t, shedding light on how complex morphological traits may be regulated through the parallel coordination of downstream target genes.

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From simplicity to complexity: The gain or loss of spot rows underlies the morphological diversity of threeDrosophilaspecies

Cited by 2 publications

References 46 publications

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

The regulation of a pigmentation gene in the formation of complex color patterns inDrosophilaabdomens

The Genetic Mechanisms Underlying the Concerted Expression of the <em>Yellow</em> and <em>Tan</em> Genes in Complex Patterns on the Abdomen and Wings of <em>Drosophila Guttifera</em>

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