Transcriptomics identifies key defense mechanisms in rice resistant to both leaf-feeding and phloem feeding herbivores.

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.

Pyramiding BPH genes in rice maintains resistance against the brown planthopper under climate change.

BACKGROUND: Nilaparvata lugens (brown planthopper; BPH) is a significant rice pest in Asia, causing substantial yield losses. Pyramiding BPH resistance genes with diverse resistance traits into rice cultivars is an effective strategy for pest management. However, the response of pyramiding combinations to environmental changes remains unclear. To address this knowledge gap, we investigated three pyramiding rice lines (BPH2 + 32, BPH9 + 32, and BPH18 + 32) in the context of varying climate change conditions, ensuring sufficient N. lugens-rice interactions. Thus, we set three environmental conditions [30/25 °C (day/night) with 500 ppm CO2 concentration, 32/27 °C (day/night) with 600 ppm CO2 concentration, and 35/30 °C (day/night) with 1000 ppm CO2 concentration]. RESULTS: All three pyramiding rice lines maintained the insect resistant ability under the three environmental settings. In particular, the BPH18 + 32 rice line exhibited stronger antibiotic and antixenosis effects against N. lugens. In addition, BPH18 + 32 rice line had better shoot resilience under N. lugens infestation, whereas the performance of the other two selected pyramiding rice lines varied. Thus, although BPH2, BPH9, and BPH18 represent three alleles at the same locus, their resistance levels against N. lugens may vary under distinct climate change scenarios, as evidenced by the performance of N. lugens on the three pyramiding rice lines. CONCLUSION: Our findings indicate that all three tested pyramiding rice lines maintained their insect resistance in the face of diverse climate change scenarios. However, these lines exhibited varied repellent responses and resilience capacities in response to climate change. Thus, the combination of pyramiding genes needs to be considered for future breeding programs. © 2023 Society of Chemical Industry.

Effect of nitrogen fertilizer on the resistance of rice near-isogenic lines with BPH resistance genes.

BACKGROUND: Nitrogen is an essential macronutrient for plant growth and development. Crops with a high nitrogen input usually have high yields. However, outbreaks of brown planthoppers (Nilaparvata lugens; BPH) frequently occur on rice farms with excessive nitrogen inputs. Rice plants carrying BPH resistance genes are used for integrated pest management. Thus, the impact of nitrogen on the resistance of rice near-isogenic lines (NILs) with BPH resistance genes was investigated. RESULTS: We tested these NILs using a standard seedbox screening test and a modified bulk seedling test under different nitrogen treatments. The amount of nitrogen applied had an impact on the resistance of some lines with BPH resistance genes. In addition, three NILs (NIL-BPH9, NIL-BPH17, and NIL-BPH32) were further examined for antibiosis and antixenosis under varying nitrogen regimes. The N. lugens nymph population growth rate, honeydew excretion, female fecundity, and nymph survival rate on the three NILs were not affected by different nitrogen treatments except the nymph survival rate on NIL-BPH9 and the nymph population growth rate on NIL-BPH17. Furthermore, in the settlement preference test, the preference of N. lugens nymphs for IR24 over NIL-BPH9 or NIL-BPH17 increased under the high-nitrogen regime, whereas the preference of N. lugens nymphs for IR24 over NIL-BPH32 was not affected by the nitrogen treatments. CONCLUSIONS: Our results indicated that the resistance of three tested NILs did not respond to different nitrogen regimes and that NIL-BPH17 exerted the most substantial inhibitory effect on N. lugens growth and development.

The Impact of Climate Change on the Resistance of Rice Near-Isogenic Lines with Resistance Genes Against Brown Planthopper.

BACKGROUND: The impact of climate change on insect resistance genes is elusive. Hence, we investigated the responses of rice near-isogenic lines (NILs) that carry resistance genes against brown planthopper (BPH) under different environmental conditions. RESULTS: We tested these NILs under three environmental settings (the atmospheric temperature with corresponding carbon dioxide at the ambient, year 2050 and year 2100) based on the Intergovernmental Panel on Climate Change prediction. Comparing between different environments, two of nine NILs that carried a single BPH-resistant gene maintained their resistance under the environmental changes, whereas two of three NILs showed gene pyramiding with two maintained BPH resistance genes despite the environmental changes. In addition, two NILs (NIL-BPH17 and NIL-BPH20) were examined in their antibiosis and antixenosis effects under these environmental changes. BPH showed different responses to these two NILs, where the inhibitory effect of NIL-BPH17 on the BPH growth and development was unaffected, while NIL-BPH20 may have lost its resistance during the environmental changes. CONCLUSION: Our results indicate that BPH resistance genes could be affected by climate change. NIL-BPH17 has a strong inhibitory effect on BPH feeding on phloem and would be unaffected by environmental changes, while NIL-BPH20 would lose its ability during the environmental changes.

Genomic and phenotypic evaluation of rice susceptible check TN1 collected in Taiwan.

BACKGROUND: Taichung Native 1 (TN1), a variety of rice (Oryza sativa L.) developed in Taiwan, has played a key role in the green revolution of this major staple crop because of its semi-dwarf characteristics. Due to its susceptibility, it has been used as a susceptibility indicator in rice insect and pathogen resistance studies worldwide. While within-variety differences have been reported for agronomic traits in other rice varieties, no study has addressed the within-variety consistency of pathogen and insect susceptibility of TN1, which would influence the result interpretation of plant-pest interaction studies. Therefore, the objective of this study was to evaluate the genomic consistency and to assess a range of agronomic and insect susceptibility traits in three representative accessions of TN1 in Taiwan. RESULTS: Among these three accessions, two were identical across 43,325 genome-wide single nucleotide polymorphisms (SNPs) while the third one differed at four SNPs. Of the three accessions of TN1, there were minor differences in seed length, seed breadth, length/width ratio, number of leaves and tillers, and number of unfilled seeds. Besides, there was no effect on relative growth rate of Cnaphalocrocis medinalis larvae fed on the three accession sources. Furthermore, there is no different on plant susceptibility among these three accessions against C. medinalis and Nilaparvata lugens. CONCLUSION: Our study indicates that it is appropriate to use TN1 in Taiwan to test for rice insect susceptibility as it yields consistent results.