Comparative Transcriptome Analysis of Juniper Branches Infected by Gymnosporangium Spp. Highlights Their Different Infection Strategies Associated with Cytokinins

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2023 Apr 5

PMID 37020280

Authors

Chenxi Shao

Siqi Tao

Yingmei Liang

Affiliations

Soon will be listed here.

Abstract

Background: Gymnosporangium asiaticum and G. yamadae can share Juniperus chinensis as the telial host, but the symptoms are completely different. The infection of G. yamadae causes the enlargement of the phloem and cortex of young branches as a gall, but not for G. asiaticum, suggesting that different molecular interaction mechanisms exist the two Gymnosporangium species with junipers.

Results: Comparative transcriptome analysis was performed to investigate genes regulation of juniper in responses to the infections of G. asiaticum and G. yamadae at different stages. Functional enrichment analysis showed that genes related to transport, catabolism and transcription pathways were up-regulated, while genes related to energy metabolism and photosynthesis were down-regulated in juniper branch tissues after infection with G. asiaticum and G. yamadae. The transcript profiling of G. yamadae-induced gall tissues revealed that more genes involved in photosynthesis, sugar metabolism, plant hormones and defense-related pathways were up-regulated in the vigorous development stage of gall compared to the initial stage, and were eventually repressed overall. Furthermore, the concentration of cytokinins (CKs) in the galls tissue and the telia of G. yamadae was significantly higher than in healthy branch tissues of juniper. As well, tRNA-isopentenyltransferase (tRNA-IPT) was identified in G. yamadae with highly expression levels during the gall development stages.

Conclusions: In general, our study provided new insights into the host-specific mechanisms by which G. asiaticum and G. yamadae differentially utilize CKs and specific adaptations on juniper during their co-evolution.

References

Liesche J, Vincent C, Han X, Zwieniecki M, Schulz A, Gao C . The mechanism of sugar export from long conifer needles. New Phytol. 2021; 230(5):1911-1924. DOI: 10.1111/nph.17302. View

Doehlemann G, Wahl R, Horst R, Voll L, Usadel B, Poree F . Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 2008; 56(2):181-195. DOI: 10.1111/j.1365-313X.2008.03590.x. View

Chen S, Zhou Y, Chen Y, Gu J . fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34(17):i884-i890. PMC: 6129281. DOI: 10.1093/bioinformatics/bty560. View

Khamis A, Chai L . Chemical and Antimicrobial Analyses of and Essential Oils and Comparison with Their Methanolic Crude Extracts. Int J Anal Chem. 2021; 2021:9937522. PMC: 8421171. DOI: 10.1155/2021/9937522. View

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth B, Remm M . Primer3--new capabilities and interfaces. Nucleic Acids Res. 2012; 40(15):e115. PMC: 3424584. DOI: 10.1093/nar/gks596. View

Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D . Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci U S A. 2006; 103(44):16598-603. PMC: 1637627. DOI: 10.1073/pnas.0603522103. View

Ren B, Wang X, Duan J, Ma J . Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation. Science. 2019; 365(6456):919-922. DOI: 10.1126/science.aav8907. View

Saur I, Huckelhoven R . Recognition and defence of plant-infecting fungal pathogens. J Plant Physiol. 2020; 256:153324. DOI: 10.1016/j.jplph.2020.153324. View

Altschul S, Gish W, Miller W, Myers E, Lipman D . Basic local alignment search tool. J Mol Biol. 1990; 215(3):403-10. DOI: 10.1016/S0022-2836(05)80360-2. View

10.

Fu L, Niu B, Zhu Z, Wu S, Li W . CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012; 28(23):3150-2. PMC: 3516142. DOI: 10.1093/bioinformatics/bts565. View

11.

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

12.

Jahn L, Hofmann U, Ludwig-Muller J . Indole-3-Acetic Acid Is Synthesized by the Endophyte via a Tryptophan-Dependent and -Independent Way and Mediates the Interaction with a Non-Host Plant. Int J Mol Sci. 2021; 22(5). PMC: 7961953. DOI: 10.3390/ijms22052651. View

13.

Chanclud E, Kisiala A, Emery N, Chalvon V, Ducasse A, Romiti-Michel C . Cytokinin Production by the Rice Blast Fungus Is a Pivotal Requirement for Full Virulence. PLoS Pathog. 2016; 12(2):e1005457. PMC: 4765853. DOI: 10.1371/journal.ppat.1005457. View

14.

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

15.

Schwacke R, Ponce-Soto G, Krause K, Bolger A, Arsova B, Hallab A . MapMan4: A Refined Protein Classification and Annotation Framework Applicable to Multi-Omics Data Analysis. Mol Plant. 2019; 12(6):879-892. DOI: 10.1016/j.molp.2019.01.003. View

16.

Martinson E, Werren J, Egan S . Tissue-specific gene expression shows a cynipid wasp repurposes oak host gene networks to create a complex and novel parasite-specific organ. Mol Ecol. 2021; 31(11):3228-3240. DOI: 10.1111/mec.16159. View

17.

Korgaonkar A, Han C, Lemire A, Siwanowicz I, Bennouna D, Kopec R . A novel family of secreted insect proteins linked to plant gall development. Curr Biol. 2021; 31(9):1836-1849.e12. PMC: 8119383. DOI: 10.1016/j.cub.2021.01.104. View

18.

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

19.

Dorostkar S, Dadkhodaie A, Ebrahimie E, Heidari B, Ahmadi-Kordshooli M . Comparative transcriptome analysis of two contrasting resistant and susceptible Aegilops tauschii accessions to wheat leaf rust (Puccinia triticina) using RNA-sequencing. Sci Rep. 2022; 12(1):821. PMC: 8764039. DOI: 10.1038/s41598-021-04329-x. View

20.

Hacquard S, Petre B, Frey P, Hecker A, Rouhier N, Duplessis S . The poplar-poplar rust interaction: insights from genomics and transcriptomics. J Pathog. 2012; 2011:716041. PMC: 3335510. DOI: 10.4061/2011/716041. View