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Insect Transcription Factors: a Landscape of Their Structures and Biological Functions in Drosophila and Beyond

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Insect Transcription Factors: a Landscape of Their Structures and Biological Functions in Drosophila and Beyond International Journal of Molecular Sciences Review Insect Transcription Factors: A Landscape of Their Structures and Biological Functions in Drosophila and beyond Zhaojiang Guo 1,† , Jianying Qin 1,2,†, Xiaomao Zhou 2 and Youjun Zhang 1,* 1 Department of Plant Protection, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China; [email protected] (Z.G.); [email protected] (J.Q.) 2 Longping Branch, Graduate School of Hunan University, Changsha 410125, China; [email protected] * Correspondence: [email protected]; Tel.: +86-10-82109518 † These authors contributed equally to this work. Received: 23 October 2018; Accepted: 16 November 2018; Published: 21 November 2018 Abstract: Transcription factors (TFs) play essential roles in the transcriptional regulation of functional genes, and are involved in diverse physiological processes in living organisms. The fruit fly Drosophila melanogaster, a simple and easily manipulated organismal model, has been extensively applied to study the biological functions of TFs and their related transcriptional regulation mechanisms. It is noteworthy that with the development of genetic tools such as CRISPR/Cas9 and the next-generation genome sequencing techniques in recent years, identification and dissection the complex genetic regulatory networks of TFs have also made great progress in other insects beyond Drosophila. However, unfortunately, there is no comprehensive review that systematically summarizes the structures and biological functions of TFs in both model and non-model insects. Here, we spend extensive effort in collecting vast related studies, and attempt to provide an impartial overview of the progress of the structure and biological functions of current documented TFs in insects, as well as the classical and emerging research methods for studying their regulatory functions. Consequently, considering the importance of versatile TFs in orchestrating diverse insect physiological processes, this review will assist a growing number of entomologists to interrogate this understudied field, and to propel the progress of their contributions to pest control and even human health. Keywords: insect; transcription factors; structures and functions; research methods; progress and prospects 1. Introduction Transcription factors (TFs) are a plethora of proteins that are present in all living organisms, and they can intricately control transcription of different functional genes in response to internal physiological processes, as well as external environmental stimuli [1,2]. Strikingly, it has been estimated that TFs make up approximately 3.5–7.0% of the total number of coding sequences in a reference eukaryotic genome [3,4]. TFs can be divided into diverse classes based on their structural characteristics, and they can influence the transcription of their targets in different mode of actions [5,6]. Most eukaryotic TFs with a DNA-binding domain (DBD) are thought to exert regulatory functions by binding to enhancers and recruiting transcriptional complexes or cofactors [7]. Nevertheless, recent studies have shown that some TFs do not perform the classical functions of binding enhancers and recruiting transcriptional complexes, but rather merely promote regulatory elements such as enhancers and promoters to form looped structures to facilitate transcriptional regulation [8]. TFs have a significant level of functional diversity, and they participate in various biological processes Int. J. Mol. Sci. 2018, 19, 3691; doi:10.3390/ijms19113691 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2018, 19, 3691 2 of 33 Int. J. Mol. Sci. 2018, 19, x FOR PEER REVIEW 2 of 32 that are pivotal to ensure the proper expression levels of targets in the appropriate time and tissue in organisms.biological processes that are pivotal to ensure the proper expression levels of targets in the Toappropriate date, there time are and several tissue reviews in organisms. summarizing the role of certain TF families in certain biochemical processes in insects, especially in Drosophila [2,9–12]. In recent years, the vast range of available To date, there are several reviews summarizing the role of certain TF families in certain genomebiochemical resources processes and novel in insects, genetic especially methods in greatly Drosophila promote [2,9–12]. the In identification recent years, the and vast investigation range of of regulatoryavailable mechanisms genome resources of TFs inand diverse novel insectsgenetic beyondmethodsDrosophila greatly promote, especially the identification lepidopteran and insects (Figureinvestigation1). However, of thereregulatory is no comprehensivemechanisms of reviewTFs in coveringdiverse insects TF structures beyond andDrosophila functions, especially in different physiologicallepidopteran and insects biochemical (Figure processes1). However, in Drosophilathere is no comprehensiveand beyond. Herein,review covering this review TF structures describes the structuresand functions of the dominating in different TFphysiological types existing and inbiochemical insects, and processes presents in aDrosophila comprehensive and beyond. summary of theHerein, roles ofthis these review TFs describes in various the insect structures biological of the processes, dominating which TF types provides existing new in insightsinsects, and into the studiespresents of transcriptional a comprehensive regulation summary in of both the roles model of th andese non-modelTFs in various insects, insect andbiological elaborates processes, on their which provides new insights into the studies of transcriptional regulation in both model and application prospects as potential new strategies for pest control in the field, and even as potential non-model insects, and elaborates on their application prospects as potential new strategies for pest targets for human disease treatment and health care. control in the field, and even as potential targets for human disease treatment and health care. Bombyx mori Keap1 MHR4 Spodoptera frugiperda Drosophila Dichaete Kr-h1 Svp Rel2 Vri melanogaster Abd-A Kr Lolal Tgo Ubx Bicyclus anynana Abd-B Dif Abd-B Kr-h1 Trh Antp Dimm l'sc Twi Antp MBF2 Plodia interpunctella Ubx AhR, ARNT Dip3 Islet, Lim3 Met EcR Amos Tll EcR-B1 Neuroptera Max Ato Dl Toy MIC E75B Ostrinia scapulalis Antp Met Apt-like Dm Tsh Odd HR3 Dsx Ase Mid Awh Papilio Xuthus dMyd Ubx Otd Antheraea assama Blattaria Thysanoptera Mitf USF BCFI, BCFII Pitx E75 ATF-2 Dnato3 (Fer3) Mld Dsx Sal Ato Dpn Vri BMFA POU-M1 Pieris rapae Chrysopa perla Mlx Vvl Atf3 Dsx BrC Rel Antheraea mylitta Blattella germanica Sal Thermobia domestica Br-C dMnt Woc Run Met, Kr-h1, E93 Bcd Dys Cad Dsx Plutella xylostella E75 Zfh1, Zfh2 Sage Svp, FTZ-F1 Nej CbZ HR3 Bmx E75 Scr Abd-A Odd Zld Antheraea pernyi EcR, USP C/EBP SGF 1/2/3/4 Lepidoptera BrC Oli Aedes aegypti CREB Diptera CncC Nine Sox genes Btd Emc Otd ATF-2, THAP E2F4 CREB Ubx Cad Ems Pb Dsx Dimm Usp Cato En, Nej Pdm1/2 βFTZ-F1 Vvl Erm Pdp1 Dsx Hemiptera Insect TF C/EBP (Slbo) HR3 PntP1 E74 Eya HNF4 Spodoptera litura atlas CLK, CYC Fer1 Prd Hairy, Gro E75 Abd-A Nilaparvata lugens CncB Fer2 Quib Met, Kr-h1, SRC, CYC E93 C/EBP BrC, Kr-h1 Coleoptera Orthoptera CncC Fkh Rel REL1 EcR Dsx CYC Rib REL2 FOXA Col FoxL1 Emc Dsx Run Crc FOXO Helicoverpa armigera FoxL2 Apis mellifera Anopheles gambiae ERR Leptinotarsa decemlineata Sage Nkx-2.5-like Locusta migratoria CrebA Ftz Deaf1, lola AP-4 Pyrrhocoris apterus Met Scr Ets transcription FoxA Trypoxylus dichotomus Met Ftz-F1 LL3 Kr-h1 factor 3-like dCREB2 Sc (Sis-B) Eve Gce Rel Met Dsx CREB SRC REL2 Cwo Séan Fkh Prey2 SRC Onthophagus taurus Cotesia glomerata Kr-h1 Gt STAT-A/B Da Sens FoxO Vvl CLK, CYC Dsx CREB Hand Culex quinquefasciatus Cimex lectularius Tribolium castaneum Cotesia rubecula Schistocerca gregaria Dac Sim βFTZ-F1 Manduca sexta Hb BrC Sima Rel2 Met, SRC CREB EcR Dei Abd-A Dsx Hinge 1/2/3 GATAβ Sis-A Glossina morsitans Aphis gossypii Kr-h1 USP Dfd, Lab Hb Dl bHLH54F AhR, ARNT Met Slp1 FOXO, Met Antp Hymenoptera Teleogryllus emma DHR3 HR3 Laodelphax striatellus SRC HSF Sna, Esg, Wor E75 Sarcophaga peregrina Vvl EcR DHR4 Hth, Tsh HR38 Fkh Tim SREBP SRAM Acyrthosiphon pisum ERR DHR39 HSF GATA-1 Allomyrina dichotoma Kni Ss Sciara Cad ILF MHR3 RelA DHR96 Kr STAT Dsx FigureFigure 1. The 1. The insect insect transcription transcription factor factor (TF) (TF) atlas,atlas, including the the well-studied well-studied TFs TFs andand their their related related referencesreferences collected collected in in the the review review (See Table Table S1 S1 for for more more detailed detailed information information about these about TFs, these and TFs, and wewe apologize to to researchers researchers whose whose work work could couldnot be notdiscussed be discussed and cited and in the cited main in text the due main to text space limitations). As yet, diverse TFs have been documented in at least nine different insect orders due to space limitations). As yet, diverse TFs have been documented in at least nine different insect including Diptera, Hemiptera, Lepidoptera, Coleoptera, Orthoptera, Thysanoptera, Blattaria, orders including Diptera, Hemiptera, Lepidoptera, Coleoptera, Orthoptera, Thysanoptera, Blattaria, Neuroptera, and Hymenoptera. Different insect species are also denoted by colored circles on the Neuroptera,vertical line. and Hymenoptera. Different insect species are also denoted by colored circles on the vertical line. 2. Structures 2. Structures Most TFs contain a DNA-binding domain (DBD) that specifically
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