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Methyl jasmonate treatment, aphid resistance assay, and transcriptomic analysis revealed different herbivore defensive roles between tobacco glandular and non-glandular trichomes

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Abstract

Key Message

Methyl jasmonate treatment and aphid resistance assays reveal different roles in herbivore defensive responses between tobacco glandular and non-glandular trichomes. These roles correlate with trichome gene expression patterns.

Abstract

In plants, trichomes greatly contribute to biotic stress resistance. To better understand the different defensive functions between glandular and non-glandular trichomes, we used Nicotiana tabacum as a model. This species bears three types of trichomes: long and short stalk glandular trichomes (LGT and SGT, respectively), and non-glandular trichomes (NGT). Tobacco accession T.I.1068 (lacking NGT) and T.I.1112 (lacking LGT) were used for the experiment. After methyl jasmonate (MeJA) treatment, LGT formation was promoted not only in T.I.1068, but also in T.I.1112, whereas NGT remained absent in T.I.1068, and was slightly reduced in T.I.1112. Diterpenoids, which play important roles in herbivore resistance, accumulated abundantly in T.I.1068 and were elevated by MeJA; however, they were not found in T.I.1112 but became detectable after MeJA treatment. The aphid resistance of T.I.1068 was higher than that of T.I.1112, and both were enhanced by MeJA, which was closely correlated with LGT density. Trichomes detached from T.I.1068 and T.I.1112 were used for RNA-Seq analysis, the results showed that pentose phosphate, photosynthesis, and diterpenoid biosynthesis genes were much more expressed in T.I.1068 than in T.I.1112, which was consistent with the vigorous diterpenoid biosynthesis in T.I.1068. In T.I.1112, citrate cycle, propanoate, and glyoxylate metabolism processes were enriched, and some defensive protein genes were expressed at higher levels than those in T.I.1068.These results suggested that LGT plays a predominant role in aphid resistance, whereas NGT could strengthen herbivore resistance by accumulating defensive proteins, and the roles of LGT and NGT are associated with their gene expression patterns.

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Availability of data and materials

All data generated or analyzed during this study are included in this published article (and its supplementary information files). The raw filtered RNA-seq data used in this article are available in the NCBI Sequence Read Archive (SRA) (https://www.ncbi.nlm.nih.gov/sra/) under BioProject accession: PRJNA577245.

Abbreviations

DEG:

Differentially Expressed Gene

ESEM:

Environmental Scanning Electron Microscopy

GC–MS:

Gas Chromatography-Mass Spectrometry

HPLC–MS/MS:

High-performance liquid chromatography-tandem mass spectrometry

LGT:

Long stalk Glandular Trichome

MeJA:

Methyl Jasmonate

MEP:

2-C-methyl-D-erythritol 4-phosphate pathway

MVA:

Mevalonate pathway

NGT:

Non-Glandular Trichome

PCA:

Principal component analysis

SGT:

Short stalk Glandular Trichome

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Funding

This research was funded by the Natural Science Foundation of Henan province [Grant No. 182300410094], the State Tobacco Monopoly Administration of China [Grant No. 110202101005 (JY-05)], and China Tobacco Henan Industrial Co., Ltd. [Grant No. AW202149].

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Authors and Affiliations

  1. College of Tobacco Science, Henan Agricultural University, 63 Nongye Road, Zhengzhou, 450002, China

    Zhaojun Wang, Yanhua Li, Hongying Zhang, Xiaoxiao Yan & Hong Cui

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  1. Zhaojun Wang
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  2. Yanhua Li
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  3. Hongying Zhang
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  4. Xiaoxiao Yan
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Contributions

HC and ZW designed the research. ZW, YL and HZ performed the aphid resistance analysis. XY observed the trichomes. ZW analyzed the RNA-Seq data. ZW and HC wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Hong Cui.

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Communicated by Da-Bing Zhang.

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Supplementary Information

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299_2021_2801_MOESM1_ESM.jpg

Supplementary Fig. S1 Environmental scanning electron microscope (ESEM) micrographs of trichomes collected from (A) T.I.1068 and (B) T.I.1112 (JPG 1720 KB)

299_2021_2801_MOESM2_ESM.jpg

Supplementary Fig. S2 Environmental scanning electron microscope (ESEM) micrographs of leaf trichomes on T.I.1068 and T.I.1112. (A) Trichomes in T.I.1068. (B) Zoomed view of long stalk glandular trichomes (LGT) in T.I.1068. (C) Trichomes in T.I.1112. (D) Zoomed view of short stalk glandular trichomes (SGT) and non-glandular trichomes (NGT) in T.I.1112 (JPG 1081 KB)

299_2021_2801_MOESM3_ESM.tif

Supplementary Fig. S3 Heat map of gene expression difference in jasmonic acid (JA) biosynthesis pathways between T.I.1068 and T.I.1112 (A) and endogenous jasmonic acid (JA) content of T.I.1068 and T.I.1112 (B). The genes expressed higher in T.I.1068 are shown in red with a color scale to indicate log2-fold changes. 13-LOX, 13-lipoxygenase; AOS, allene oxide synthase; AOC, allene oxide cyclase; OPR3, ( +)-12-oxo-phytodienoic acid reductase 3; OPCL1, 3-oxo-2-( 2-pentenyl)-cyclopentane-1-octanoyl-CoA ligase 1; ACX, acyl-CoA oxidase; MFP, multifunctional protein with 2-trans-enoyl-CoA hydratase and L-3-hydroxyacyl-CoA dehydrogenase activity; KAT, 3-ketoacyl-CoA thiolase (TIF 1829 KB)

Supplementary Table S1 Genes selected and primers used for qRT-PCR (XLS 28 KB)

Supplementary Table S2 Summary of RNA-Seq reads for T.I.1068 and T.I.1112 detached trichomes (DOC 35 KB)

299_2021_2801_MOESM6_ESM.xlsx

Supplementary Table S3 The list of differentially expressed genes (DEGs) more expressed in T.I.1068 than in T.I.1112 (XLSX 489 KB)

299_2021_2801_MOESM7_ESM.xlsx

Supplementary Table S4 The list of differentially expressed genes (DEGs) more expressed in T.I.1112 than in T.I.1068 (XLSX 465 KB)

299_2021_2801_MOESM8_ESM.xls

Supplementary Table S5 The list of all KEGG pathways of the differentially expressed genes (DEGs) more expressed in T.I.1068 than in T.I.1112 (XLS 70 KB)

299_2021_2801_MOESM9_ESM.xls

Supplementary Table S6 The list of all KEGG pathways of the differentially expressed genes (DEGs) more expressed in T.I.1112 than in T.I.1068 (XLS 78 KB)

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Wang, Z., Li, Y., Zhang, H. et al. Methyl jasmonate treatment, aphid resistance assay, and transcriptomic analysis revealed different herbivore defensive roles between tobacco glandular and non-glandular trichomes. Plant Cell Rep 41, 195–208 (2022). https://doi.org/10.1007/s00299-021-02801-6

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