Exploring the Diversity of Galls on Induced by Species Through Morphological and Transcriptome Analyses

Overview

Journal Plant Direct

Specialty Biology

Date 2024 Jul 4

PMID 38962171

Authors

Seiji Takeda

Makiko Yoza

Sawako Ueda

Sakura Takeuchi

Akiteru Maeno

Tomoaki Sakamoto

Seisuke Kimura

Affiliations

Soon will be listed here.

Abstract

Plant galls generated by insects have highly organized structures, providing nutrients and shelter to the insects living within them. Most research on the physiological and molecular mechanisms of gall development has focused on single galls. To understand the diversity of gall development, we examined five galls with different morphologies generated by distinct species of (gall midge; Diptera: Cecidomyiidae) on a single host plant of var. (Asteraceae). Vasculature developed de novo within the galls, indicating active transport of nutrients between galls and the host plant. Each gall had a different pattern of vasculature and lignification, probably due to differences in the site of gall generation and the gall midge species. Transcriptome analysis indicated that photosynthetic and cell wall-related genes were down-regulated in leaf and stem galls, respectively, compared with control leaf and stem tissues, whereas genes involved in floral organ development were up-regulated in all types of galls, indicating that transformation from source to sink organs occurs during gall development. Our results help to understand the diversity of galls on a single herbaceous host plant.

Citing Articles

Morphological and Transcriptome Analysis of the Near-Threatened Orchid with Petals Shaped Like a Flying White Bird.

Takeda S, Nishikawa Y, Tachibana T, Higaki T, Sakamoto T, Kimura S Plants (Basel). 2025; 14(3).

PMID: 39942954 PMC: 11820888. DOI: 10.3390/plants14030393.

References

Thomas P, Ebert D, Muruganujan A, Mushayahama T, Albou L, Mi H . PANTHER: Making genome-scale phylogenetics accessible to all. Protein Sci. 2021; 31(1):8-22. PMC: 8740835. DOI: 10.1002/pro.4218. View

Nakata M, Mitsuda N, Herde M, Koo A, Moreno J, Suzuki K . A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in arabidopsis. Plant Cell. 2013; 25(5):1641-56. PMC: 3694697. DOI: 10.1105/tpc.113.111112. View

Gu Q, Ferrandiz C, Yanofsky M, Martienssen R . The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development. 1998; 125(8):1509-17. DOI: 10.1242/dev.125.8.1509. View

Sorensen A, Krober S, Unte U, Huijser P, Dekker K, Saedler H . The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 2003; 33(2):413-23. DOI: 10.1046/j.1365-313x.2003.01644.x. View

Staedler Y, Masson D, Schonenberger J . Plant tissues in 3D via X-ray tomography: simple contrasting methods allow high resolution imaging. PLoS One. 2013; 8(9):e75295. PMC: 3785515. DOI: 10.1371/journal.pone.0075295. View

Hsieh W, Hsieh H, Wu S . Arabidopsis bZIP16 transcription factor integrates light and hormone signaling pathways to regulate early seedling development. Plant Cell. 2012; 24(10):3997-4011. PMC: 3517232. DOI: 10.1105/tpc.112.105478. View

Hardtke C, Berleth T . The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 1998; 17(5):1405-11. PMC: 1170488. DOI: 10.1093/emboj/17.5.1405. View

Schultz J, Edger P, Body M, Appel H . A galling insect activates plant reproductive programs during gall development. Sci Rep. 2019; 9(1):1833. PMC: 6372598. DOI: 10.1038/s41598-018-38475-6. View

Degenhardt K, Wright A, Horng D, Padmanabhan A, Epstein J . Rapid 3D phenotyping of cardiovascular development in mouse embryos by micro-CT with iodine staining. Circ Cardiovasc Imaging. 2010; 3(3):314-22. PMC: 3059892. DOI: 10.1161/CIRCIMAGING.109.918482. View

10.

Takeda S, Yoza M, Amano T, Ohshima I, Hirano T, Sato M . Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development. PLoS One. 2019; 14(10):e0223686. PMC: 6812778. DOI: 10.1371/journal.pone.0223686. View

11.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

12.

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

13.

Hirano T, Kimura S, Sakamoto T, Okamoto A, Nakayama T, Matsuura T . Reprogramming of the Developmental Program of During Initial Stage of Gall Induction by . Front Plant Sci. 2020; 11:471. PMC: 7243852. DOI: 10.3389/fpls.2020.00471. View

14.

Harris M, Pitzschke A . Plants make galls to accommodate foreigners: some are friends, most are foes. New Phytol. 2019; 225(5):1852-1872. DOI: 10.1111/nph.16340. View

15.

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(2):586-595. DOI: 10.1111/j.1469-8137.2012.04264.x. View

16.

Chen H, Liu J, Cui K, Lu Q, Wang C, Wu H . Molecular mechanisms of tannin accumulation in Rhus galls and genes involved in plant-insect interactions. Sci Rep. 2018; 8(1):9841. PMC: 6026138. DOI: 10.1038/s41598-018-28153-y. View

17.

Tamura K . Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol. 1992; 9(4):678-87. DOI: 10.1093/oxfordjournals.molbev.a040752. View

18.

Brunner A, Yakovlev I, Strauss S . Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol. 2004; 4:14. PMC: 515301. DOI: 10.1186/1471-2229-4-14. View

19.

Skuhrava M, Massa B, Cerasa G . Rediscovery and identity of Pumilomyia protrahenda De Stefani (Diptera, Cecidomyiidae) in Sicily with redescription and reassessment of its taxonomic position. Zookeys. 2016; (617):129-37. PMC: 5027773. DOI: 10.3897/zookeys.617.9850. View

20.

Sawa S, Watanabe K, Goto K, Liu Y, Shibata D, Kanaya E . FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 1999; 13(9):1079-88. PMC: 316944. DOI: 10.1101/gad.13.9.1079. View