Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development


Autoři: Seiji Takeda aff001;  Makiko Yoza aff001;  Taisuke Amano aff001;  Issei Ohshima aff001;  Tomoko Hirano aff001;  Masa H. Sato aff001;  Tomoaki Sakamoto aff003;  Seisuke Kimura aff003
Působiště autorů: Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan aff001;  Biotechnology Research Department, Kyoto Prefectural Agriculture Forestry and Fisheries Technology Center, Seika, Kyoto, Japan aff002;  Department of Bioresource and Environmental Sciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, Japan aff003;  Department of Industrial Life Sciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, Japan aff004;  Center for Ecological Evolutionary Developmental Biology, Kyoto Sangyo University, Kyoto, Japan aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223686

Souhrn

Galls are plant structures generated by gall–inducing organisms including insects, nematodes, fungi, bacteria and viruses. Those made by insects generally consist of inner callus–like cells surrounded by lignified hard cells, supplying both nutrients and protection to the gall insects living inside. This indicates that gall insects hijack developmental processes in host plants to generate tissues for their own use. Although galls are morphologically diverse, the molecular mechanism for their development remains poorly understood. To identify genes involved in gall development, we performed RNA–sequencing based transcriptome analysis for leaf galls. We examined the young and mature galls of Glochidion obovatum (Phyllanthaceae), induced by the micromoth Caloptilia cecidophora (Lepidoptera: Gracillariidae), the leaf gall from Eurya japonica (Pentaphylacaceae) induced by Borboryctis euryae (Lepidoptera: Gracillariidae), and the strawberry-shaped leaf gall from Artemisia montana (Asteraceae) induced by gall midge Rhopalomyia yomogicola (Oligotrophini: Cecidomyiidae). Gene ontology (GO) analyses suggested that genes related to developmental processes are up–regulated, whereas ones related to photosynthesis are down–regulated in these three galls. Comparison of transcripts in these three galls together with the gall on leaves of Rhus javanica (Anacardiaceae), induced by the aphid Schlechtendalia chinensis (Hemiptera: Aphidoidea), suggested 38 genes commonly up–regulated in galls from different plant species. GO analysis showed that peptide biosynthesis and metabolism are commonly involved in the four different galls. Our results suggest that gall development involves common processes across gall inducers and plant taxa, providing an initial step towards understanding how they manipulate host plant developmental systems.

Klíčová slova:

Cell cycle and cell division – Gene ontologies – Insects – Leaves – Plants – RNA extraction – Transcription factors – Transcriptional control


Zdroje

1. Stone GN, Schönrogge K. The adaptive significance of insect gall morphology. Trends Ecol Evol 2003;18: 512–522. doi: 10.1016/s0169–5347(03)00247–7

2. Espírito–Santo MM, Fernandes GW. How many species of gall–inducing insects are there on earth, and where are they? Ann Entomol Soc Am. 2007;100: 95–99. doi: 10.1603/0013–8746(2007)100[95:HMSOGI:2.0.CO;2

3. Yamaguchi H, Tanaka H, Hasegawa M, Tokuda M, Asami T, Suzuki Y. Phytohormones and willow gall induction by a gall–inducing sawfly. New Phytol. 2012;196: 586–595. doi: 10.1111/j.1469-8137.2012.04264.x 22913630

4. Tanaka Y, Okada K, Asami T, Suzuki Y. Phytohormones in Japanese mugwort gall induction by a gall–inducing gall midge. Biosci Biotechnol Biochem. 2013;77: 1942–1948. doi: 10.1271/bbb.130406 24018692

5. Bartlett L, Connor EF. Exogenous phytohormones and the induction of plant galls by insects. Arthropod–Plant Interact. 2014;8: 339–348. doi: 10.10007/s11829–011–9309–0

6. Giron D, Huguet E, Stone GN, Body M. Insect–induced effects on plants and possible effectors used by galling and leaf–mining insects to manipulate their host–plant. J Insect Physiol. 2016;84: 70–89. doi: 10.1016/j.jinsphys.2015.12.009 26723843

7. Kaiser W, Huguet E, Casas J, Commin C, Giron D. Plant green–island phenotype induced by leaf–miners is mediated by bacterial symbionts. Proc R Soc B. 2010;277: 2311–2319. doi: 10.1098/rspb.2010.0214 20356892

8. Body M, Kaiser W, Dubreuil G, Casas J, Giron D. Leaf–miners co–opt microorganisms to enhance their nutritional environment. J Chem Ecol 2013;39: 969–977. doi: 10.1007/s10886-013-0307-y 23807431

9. Barnewall EC, De Clerck–Floate RA. A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod–Plant Interact. 2012;6: 449–459. doi: 10.1007/s11829–012–9193–4

10. Bailey S, Percy DM, Hefer CA, Cronk QCB. The transcriptional landscape of insect galls: psyllid (Hemiptera) gall formation in Hawaiian Metrosideros polymorpha (Myrtaceae). BMC Genomics. 2015;16: 943. doi: 10.1186/s12864-015-2109-9 26572921

11. Liu P, Yang ZX, Chen XM, Yang P. RNA–seq–based transcriptome and the reproduction–related genes for the aphid Schlechtendalia chinensis (Hemiptera, Aphididae). Genet Mol Res. 2017;16: gmr16019448. doi: 10.4238/gmr16019448 28340266

12. Chen H, Liu J, Cui K, Lu Q, Wang C, Wu H, et al. Molecular mechanisms of tannin accumulation in Rhus galls and genes involved in plant–insect interactions. Sci Rep. 2018;8: 9841. doi: 10.1038/s41598-018-28153-y 29959354

13. Schultz JC, Edger PP, Body MJA, Appel HM. A galling insect activates plant reproductive programs during gall development. Sci Rep. 2019;9: 1833. doi: 10.1038/s41598-018-38475-6 30755671

14. Guiguet A, Ohshima I, Takeda S, Laurans F, Lopez–Vaamonde C, Giron D. Origin of gall–inducing from leaf–mining in Caloptilia micromoths (Lepidoptera, Gracillariidae). Sci Rep. 2019;9: 6794. doi: 10.1038/s41598-019-43213-7 31043653

15. Guiguet A, Hamatani A, Amano T, Takeda S, Lopez–Vaamonde C, Giron D, et al. Inside the horn of plenty: leaf–mining micromoth manipulates its host plant to obtain unending food provisioning. PLoS ONE. 2018;13: e0209485. doi: 10.1371/journal.pone.0209485 30576396

16. Brunner AM, Yakovlev IA, Strauss SH. Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol. 2004;4: 1–7. doi: 10.1186/1471-2229-4-1

17. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full–length transcriptome assembly from RNA–seq data without a reference genome. Nat Biotechnol. 2011;29: 644–652. doi: 10.1038/nbt.1883 21572440

18. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009;25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

19. Robinson MD, McCarthy DJ, Smyth GK. EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308

20. Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD. PANTHER version 14: more genomes, a new PANTHER GO–slim and improvements in enrichment analysis tools. Nucleic Acids Res. 2018;47: D419–D426. doi: 10.1093/nar/gky1038 30407594

21. Lafarge S, Montané MH. Characterization of Arabidopsis thaliana ortholog of the human breast cancer susceptibility gene 1: AtBRCA1, strongly induced by gamma rays. Nucleic Acids Res. 2003;31: 1148–1155. doi: 10.1093/nar/gkg202 12582233

22. Sjogren CA, Bolaris SC, Larsen PB. Aluminum–dependent terminal differentiation of the Arabidopsis root tip is mediated through an ATR–, ALT2–, and SOG1–regulated transcriptional response. Plant Cell. 2015;27: 2501–2515. doi: 10.1105/tpc.15.00172 26320227

23. Ogita N, Okushima Y, Tokizawa M, Yamamoto YY, Tanaka M, Seki M, et al. Identifying the target genes of SUPPRESSOR OF GAMMA RESPONSE 1, a master transcription factor controlling DNA damage response in Arabidopsis. Plant J. 2018;94: 439–453. doi: 10.1111/tpj.13866 29430765

24. Oh SA, Johnson A, Smertenko A, Rahman D, Park SK, Hussey PJ, et al. A divergent cellular role for the FUSED kinase family in the plant–specific cytokinetic phragmoplast. Curr Biol. 2005;15: 2107–2111. doi: 10.1016/j.cub.2005.10.044 16332535

25. Oh SA, Allen T, Kim GJ, Sidorova A, Borg M, Park SK, et al. Arabidopsis Fused kinase and the Kinesin–12 subfamily constitute a signaling module required for phragmoplast expansion. Plant J. 2012;72: 308–319. doi: 10.1111/j.1365-313X.2012.05077.x 22709276

26. Heyman J, Cools T, Vandenbussche F, Heyndrickx KS, Leene JV, Vercauteren I, et al. ERF115 controls root quiescent center cell division and stem cell replenishment. Science 2013;342: 860–863. doi: 10.1126/science.1240667 24158907

27. Lahmy S, Guilleminot J, Cheng CM, Bechtold N, Albert S, Pelletier G, et al. DOMINO1, a member of a small plant–specific gene family, encodes a protein essential for nuclear and nucleolar functions. Plant J. 2004;39: 809–820. doi: 10.1111/j.1365-313X.2004.02166.x 15341625

28. Dubois E, Córdoba–Cañero D, Massot S, Siaud N, Gakière B, Domenichini S, et al. Homologous recombination is stimulated by a decrease in dUTPase in Arabidopsis. PLoS ONE. 2011;6: e18658. doi: 10.1371/journal.pone.0018658 21541310

29. Wang M, Xu Z, Ahmed RI, Wang Y, Hu R, Zhou G, et al. Tubby–like Protein 2 regulates homogalacturonan biosynthesis in Arabidopsis seed coat mucilage. Plant Mol Biol. 2019;99: 421–436. doi: 10.1007/s11103-019-00827-9 30707395

30. Shigeto J, Nagano M, Fujita K, Tsutsumi Y. Catalytic profile of Arabidopsis peroxidases, AtPrx–2, 25 and 71, contributing to stem lignification. PLoS ONE. 2014;9: e105332. doi: 10.1371/journal.pone.0105332 25137070

31. Shigeto J, Kiyonaga Y, Fujita K, Kondo R, Tsutsumi Y. Putative cationic cell–wall–bound peroxidase homologues in Arabidopsis, AtPrx2, AtPrx25, and AtPrx71, are involved in lignification. J Agri Food Chem. 2013;1: 3781–3788. doi: 10.1021/jf400426g 23551275

32. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 2003;22: 42–446. doi: 10.1038/nature01485 12660786

33. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. Local positive feedback regulation determines cell shape in root hair cells. Science 2008;19: 1241–1244. doi: 10.1126/science.1152505 18309082

34. Sng NJ, Kolaczkowski B, Ferl RJ, Paul AL. A member of the CONSTANS–like protein family is a putative regulator of reactive oxygen species homeostasis and spaceflight physiological adaptation. AoB Plants. 2018;11: ply075. doi: 10.1093/aobpla/ply075 30705745

35. Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, et al. The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell. 2007;19: 2440–2453. doi: 10.1105/tpc.107.050963 17675404

36. Zhao Y, Xing L, Wang X, Hou YJ, Gao J, Wang P, et al. The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77–dependent transcription of auxin–responsive genes. Sci Signal. 2015;7: ra53. doi: 10.1126/scisignal.2005051 24894996

37. Sugimoto K, Jiao Y, Meyerowitz EM. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell. 2010;18: 463–471. doi: 10.1016/j.devcel.2010.02.004 20230752

38. Grunewald W, Smet ID, Lewis DR, Löfke C, Jansen L, Goeminne G, et al. Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci USA. 2012;109: 155–1559. doi: 10.1073/pnas.1110541108

39. Grunewald W, Smet ID, Rybel BD, Robert HS, van de Cotte B, Willemesen V, et al. Tightly controlled WRKY23 expression mediates Arabidopsis embryo development. EMBO Rep. 2013;14: 1136–1142. doi: 10.1038/embor.2013.169 24157946

40. Prát T, Hajný J, Grunewald W, Vasileva M, Molnár G, Tejos R, et al. WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genet. 2018;14: e1007177. doi: 10.1371/journal.pgen.1007177 29377885

41. Grunewald W, Karimi M, Wieczorek K, de Cappelle EV, Wischnitzki E, Grundler F, et al. A role for AtWRKY23 in feeding site establishment of plant–parasitic nematodes. Plant Physiol. 2008;148: 358–368. doi: 10.1104/pp.108.119131 18599655

42. Gardiner J, Sherr I, Scarpella E. Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol 2010;54: 1389–1396, doi: 10.1387/ijdb.093006jg 20563990

43. Werner T, Schmülling T. Cytokinin action in plant development. Curr Opin Plant Biol. 2009;12: 527–538. doi: 10.1016/j.pbi.2009.07.002 19740698

44. D´Agostino IB, Deruère J, Kieber JJ. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 2000;124: 1706–1717 doi: 10.1104/pp.124.4.1706 11115887

45. Rashotte AM, Carson SDB, To JPC, Kieber JJ. Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 2003;132: 1998–2011. doi: 10.1104/pp.103.021436 12913156

46. To JPC, Haberer G, Ferreira FJ, Druère J, Mason MG, Schaller GE, et al. Type–A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 2004;16: 658–671. doi: 10.1105/tpc.018978 14973166

47. Lorrai R, Gandolfi F, Boccaccini A, Ruta V, Possenti M, Tramontano A, et al. Genome–wide RNA–seq analysis indicates that the DAG1 transcription factor promotes hypocotyl elongation acting on ABA, ethylene and auxin signaling. Sci Rep. 2018;8: 15895. doi: 10.1038/s41598-018-34256-3 30367178

48. Papi M, Sabatini S, Bouchez D, Camilleri C, Costantino P, Vttorioso P. Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev. 2000;14: 28–33. 10640273

49. Zeilmaker T, Ludwig NR, Elberse J, Seidl MF, Berke L, Doorn AV, et al. DOWNY MILDEW RESISTANT 6 and DMR6–LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J. 2015;81: 210–222. doi: 10.1111/tpj.12719 25376907

50. Liu J, Elmore JM, Lin ZJD, Coaker G. A receptor–like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe. 2011;9: 137–146. doi: 10.1016/j.chom.2011.01.010 21320696

51. Jin J, Hewezi T, Baum TJ. The Arabidopsis bHLH25 and bHLH27 transcription factors contribute to susceptibility to the cyst nematode Heterodera schachtii. Plant J. 2011;65: 319–328. doi: 10.1111/j.1365-313X.2010.04424.x 21223395

52. Xing DH, Lai ZB, Zheng ZY, Vinod KM, Fan BF, Chen ZX. Stress–and pathogen–induced Arabidopsis WRKY48 is a transcriptional activator that represses plant basal defense. Mol Plant 2008;1: 459–470. doi: 10.1093/mp/ssn020 19825553

53. Xu Y, Yu Z, Zhang D, Huang J, Wu C, Yang G, et al. CYSTM, a novel non–secreted cysteine–rich peptide family, involved in environmental stresses in Arabidopsis thaliana. Plant Cell Physiol. 2018;59: 423–438. doi: 10.1093/pcp/pcx202 29272523

54. Chen Y, Chen Z, Kang J, Kang D, Gu H, Qin G. AtMYB14 regulates cold tolerance in Arabidopsis. Plant Mol Biol Rep. 2013;31: 87–97. doi: 10.1007/s11105-012-0481-z 24415840

55. Williams B, Kabbage M, Britt R, Dickman MB. AtBAG7, an Arabidopsis Bcl–2–associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc Natl Acad Sci USA. 2010;107: 3088–6093. doi: 10.1073/pnas.0912670107 20231441

56. Pan YJ, Liu L, Lin YC, Zu YG, Li LP, Tang ZH. Ethylene antagonizes salt–induced growth retardation and cell death process via transcriptional controlling of ethylene–, BAG–and senescence–associated genes in Arabidopsis. Frontiers Plant Sci. 2016;7: 696. doi: 10.3389/fpls.2016.00696 27242886

57. Li Y, Williams B, Dickman M. Arabidopsis B–cell lymphoma2 (Bcl–2)–associated athanogene 7 (BAG7)–mediated heat tolerance requires translocation, sumoylation and binding to WRKY29. New Phytol. 2017;214: 695–705. doi: 10.1111/nph.14388 28032645

58. Ikeda M, Mitsuda N, Ohme–Takagi M. Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat–inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol. 2011;157: 1243–1254. doi: 10.1104/pp.111.179036 21908690

59. Pick T, Jaskiewicz M, Peterhänsel C, Conrath U. Heat shock factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiol. 2012;159: 52–55. doi: 10.1104/pp.111.191841 22427343

60. Depuydt S, Rodriguez–Villalon A, Santuari L, Wyser–Rmili C, Ragni L, Hardtke CS. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor–like kinase BAM3. Proc Natl Acad Sci USA. 2013;110: 7074–7079. doi: 10.1073/pnas.1222314110 23569225

61. Hazak O, Brandt B, Cattaneo P, Santiago J, Rodriguez–Villalon A, Hothorn M, et al. Perception of root–active CLE peptide requires CORYNE function in the phloem vasculature. EMBO Rep. 2017;18: 1367–1381. doi: 10.15252/embr.201643535 28607033

62. Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, et al. A small peptide modulates stomatal control via abscisic acid in long–distance signaling. Nature 2018;556: 235–238. doi: 10.1038/s41586-018-0009-2 29618812

63. Ferrero S, Grados–Torrez RE, Leivar P, Antolín–Llovera M, López–Iglesias C, Cortadellas N. et al. Proliferation and morphogenesis of the endoplasmic reticulum driven by the membrane domain of 3–hydroxy–3–methylglutaryl coenzyme A reductase in plant cells. Plant Physiol. 2015;168: 899–914. doi: 10.1104/pp.15.00597 26015445

64. Qu Y, Egelund J, Gilson PR, Houghton F, Gleeson PA, Shultz CJ, et al. Identification of a novel group of putative Arabidopsis thaliana ß–(1,3)–galactosyltransferases. Plant Mol Biol. 2008;68: 43–59. doi: 10.1007/s11103-008-9351-3 18548197

65. Chu B, Wilson TJ, McCune–Zierath C, Snustad DP, Carter JV. Two ß–tubulin genes, TUB1 and TUB8, of Arabidopsis exhibit largely nonoverlapping patterns of expression. Plant Mol Biol. 1998;37: 785–790. doi: 10.1023/a:1006047129410 9678573

66. Voss I, Goss T, Murozuka E, Altmann B, McLean KJ, Rigby SEJ, et al. FdC1, a novel ferredoxin protein capable of alternative electron partitioning, increases in conditions of acceptor limitation at photosystem I J Biol Chem. 2011;286: 50–59. doi: 10.1074/jbc.M110.161562 20966083

67. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development. 2007;134: 1051–1060. doi: 10.1242/dev.02817 17287247

68. Liu L, Li C, Liang Z, Yu H. Characterization of multiple C2 domain and transmembrane region proteins in Arabidopsis. Plant Physiol. 2018;176: 2119–2132. doi: 10.1104/pp.17.01144 29259105

69. Ito T, Takahashi N, Shimura Y, Okada K. A serine/threonine protein kinase gene isolated by an in vivo binding procedure using the Arabidopsis floral homeotic gene product, AGAMOUS. Plant Cell Physiol. 1997;38: 248–258. doi: 10.1093/oxfordjournals.pcp.a029160 9150601

70. Yamaguchi YL, Ishida T, Sawa S. CLE peptides and their signaling pathways in plant development. J Exp Bot. 2016;67: 4813–4826. doi: 10.1093/jxb/erw208 27229733

71. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, et al. Non–cell–autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA. 2008;105: 15208–15213, doi: 10.1073/pnas.0808444105 18812507

72. Guo X, Wang J, Gardner M, Fukuda H, Kondo Y, Etchells JP, et al. Identification of cyst nematode B–type peptides and modulation of the vascular stem cell pathway for feeding cell formation. PLoS Pathog. 2017;13: e1006142. doi: 10.1371/journal.ppat.1006142 28158306

73. Hirakawa Y, Kondo Y, Fukuda H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell. 2010;22: 2618–2629. doi: 10.1105/tpc.110.076083 20729381

74. Theissen G, Saedler H. Floral quartets. Nature. 2001;409: 469–471. doi: 10.1038/35054172 11206529

75. Krizek BA, Fletcher JC. Molecular mechanisms of flower development: an armchair guide. Nat Rev. 2005;6: 688–698. doi: 10.1038/nrg1675 16151374


Článek vyšel v časopise

PLOS One


2019 Číslo 10