Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores
Abstract Background Outbreaks of insect pests in paddy fields cause heavy losses in global rice yield annually, a threat projected to be aggravated by ongoing climate warming. Although significant progress has been made in the screening and cloning of insect resistance genes in rice germplasm and th...
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doaj-16c03e69e742400bb307dd8759ca28422021-07-04T11:08:59ZengBMCBMC Plant Biology1471-22292021-06-0121111810.1186/s12870-021-03068-5Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivoresYi Li0Boon Huat Cheah1Yu-Fu Fang2Yun-Hung Kuang3Shau-Ching Lin4Chung-Ta Liao5Shou-Horng Huang6Ya-Fen Lin7Wen-Po Chuang8Department of Agronomy, National Taiwan UniversityDepartment of Agronomy, National Taiwan UniversityDepartment of Agronomy, National Taiwan UniversityDepartment of Agronomy, National Taiwan UniversityDepartment of Agronomy, National Taiwan UniversityCrop Environment Section, Taichung District Agricultural Research and Extension Station, COADepartment of Plant Protection, Chiayi Agricultural Experiment Station, Taiwan Agricultural Research Institute, Council of AgricultureDepartment of Agronomy, National Taiwan UniversityDepartment of Agronomy, National Taiwan UniversityAbstract Background Outbreaks of insect pests in paddy fields cause heavy losses in global rice yield annually, a threat projected to be aggravated by ongoing climate warming. Although significant progress has been made in the screening and cloning of insect resistance genes in rice germplasm and their introgression into modern cultivars, improved rice resistance is only effective against either chewing or phloem-feeding insects. Results In this study, the results from standard and modified seedbox screening, settlement preference and honeydew excretion tests consistently showed that Qingliu, a previously known leaffolder-resistant rice variety, is also moderately resistant to brown planthopper (BPH). High-throughput RNA sequencing showed a higher number of differentially expressed genes (DEGs) at the infestation site, with 2720 DEGs in leaves vs 181 DEGs in sheaths for leaffolder herbivory and 450 DEGs in sheaths vs 212 DEGs in leaves for BPH infestation. The leaf-specific transcriptome revealed that Qingliu responds to leaffolder feeding by activating jasmonic acid biosynthesis genes and genes regulating the shikimate and phenylpropanoid pathways that are essential for the biosynthesis of salicylic acid, melatonin, flavonoids and lignin defensive compounds. The sheath-specific transcriptome revealed that Qingliu responds to BPH infestation by inducing salicylic acid-responsive genes and those controlling cellular signaling cascades. Taken together these genes could play a role in triggering defense mechanisms such as cell wall modifications and cuticular wax formation. Conclusions This study highlighted the key defensive responses of a rarely observed rice variety Qingliu that has resistance to attacks by two different feeding guilds of herbivores. The leaffolders are leaf-feeder while the BPHs are phloem feeders, consequently Qingliu is considered to have dual resistance. Although the defense responses of Qingliu to both insect pest types appear largely dissimilar, the phenylpropanoid pathway (or more specifically phenylalanine ammonia-lyase genes) could be a convergent upstream pathway. However, this possibility requires further studies. This information is valuable for breeding programs aiming to generate broad spectrum insect resistance in rice cultivars.https://doi.org/10.1186/s12870-021-03068-5Oryza sativaCnaphalocrocis medinalisNilaparvata lugensRNA-SeqDual resistance |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Yi Li Boon Huat Cheah Yu-Fu Fang Yun-Hung Kuang Shau-Ching Lin Chung-Ta Liao Shou-Horng Huang Ya-Fen Lin Wen-Po Chuang |
spellingShingle |
Yi Li Boon Huat Cheah Yu-Fu Fang Yun-Hung Kuang Shau-Ching Lin Chung-Ta Liao Shou-Horng Huang Ya-Fen Lin Wen-Po Chuang Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores BMC Plant Biology Oryza sativa Cnaphalocrocis medinalis Nilaparvata lugens RNA-Seq Dual resistance |
author_facet |
Yi Li Boon Huat Cheah Yu-Fu Fang Yun-Hung Kuang Shau-Ching Lin Chung-Ta Liao Shou-Horng Huang Ya-Fen Lin Wen-Po Chuang |
author_sort |
Yi Li |
title |
Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores |
title_short |
Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores |
title_full |
Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores |
title_fullStr |
Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores |
title_full_unstemmed |
Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores |
title_sort |
transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores |
publisher |
BMC |
series |
BMC Plant Biology |
issn |
1471-2229 |
publishDate |
2021-06-01 |
description |
Abstract Background Outbreaks of insect pests in paddy fields cause heavy losses in global rice yield annually, a threat projected to be aggravated by ongoing climate warming. Although significant progress has been made in the screening and cloning of insect resistance genes in rice germplasm and their introgression into modern cultivars, improved rice resistance is only effective against either chewing or phloem-feeding insects. Results In this study, the results from standard and modified seedbox screening, settlement preference and honeydew excretion tests consistently showed that Qingliu, a previously known leaffolder-resistant rice variety, is also moderately resistant to brown planthopper (BPH). High-throughput RNA sequencing showed a higher number of differentially expressed genes (DEGs) at the infestation site, with 2720 DEGs in leaves vs 181 DEGs in sheaths for leaffolder herbivory and 450 DEGs in sheaths vs 212 DEGs in leaves for BPH infestation. The leaf-specific transcriptome revealed that Qingliu responds to leaffolder feeding by activating jasmonic acid biosynthesis genes and genes regulating the shikimate and phenylpropanoid pathways that are essential for the biosynthesis of salicylic acid, melatonin, flavonoids and lignin defensive compounds. The sheath-specific transcriptome revealed that Qingliu responds to BPH infestation by inducing salicylic acid-responsive genes and those controlling cellular signaling cascades. Taken together these genes could play a role in triggering defense mechanisms such as cell wall modifications and cuticular wax formation. Conclusions This study highlighted the key defensive responses of a rarely observed rice variety Qingliu that has resistance to attacks by two different feeding guilds of herbivores. The leaffolders are leaf-feeder while the BPHs are phloem feeders, consequently Qingliu is considered to have dual resistance. Although the defense responses of Qingliu to both insect pest types appear largely dissimilar, the phenylpropanoid pathway (or more specifically phenylalanine ammonia-lyase genes) could be a convergent upstream pathway. However, this possibility requires further studies. This information is valuable for breeding programs aiming to generate broad spectrum insect resistance in rice cultivars. |
topic |
Oryza sativa Cnaphalocrocis medinalis Nilaparvata lugens RNA-Seq Dual resistance |
url |
https://doi.org/10.1186/s12870-021-03068-5 |
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