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 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.

The Effect of Antibiotic Treatment on the Bacterial Community of the Brown Planthopper and Its Correlation with Rice Virulence

“…A recent study showed that a rice variety from Taiwan, Qingliu, displays a rarely observed dual resistance to the leaffolder (chewing insect) and the BPH. Although the responses of Qingliu to both insect pests appear vastly dissimilar, the phenylpropanoid pathway could be a convergent upstream pathway [65]. This study showed that the phenylpropanoid pathway is valuable for generating broad-spectrum resistance in rice cultivars.…”

Early transcriptomic responses of rice leaves to herbivory by Spodoptera frugiperda

“…OsBURP genes are known to play a role in plant vegetative and reproductive development and in tolerance to abiotic stresses (drought, salt stress, aluminum and cold) and respond to ABA 90 . In addition, OsBURP02 and OsBURP07 are induced 24 h after infestation by rice leafolder ( Cnaphalocrocis medinalis , Guenée, 1854, chewing insect) and brown planthopper ( Nilparvata lugens , Stahl, 1854, piercing-sucking insect) 33 . In rice, this induction of OsBURP might be prevented by the OS microbiota.…”

Expression Analysis Reveals Differentially Expressed Genes in BPH and WBPH Associated with Resistance in Rice RILs Derived from a Cross between RP2068 and TN1

“…During its evolutionary history, rice has developed several defense mechanisms against BPH, WBPH, and several other invaders [ 10 , 27 ]. Resistance to BPH is complex as it involves multiple sophisticated regulatory mechanisms both at the level of the insect and its host [ 28 ].…”