Genome-wide analysis of cotton miRNAs during whitefly infestation offers new insights into plant-herbivore interaction

Authors: LI, JIANYING - Huazhong Agricultural University; Hull, Joe; LIANG, SIJIA - Huazhong Agricultural University; WANG, QIONGQIONG - Huazhong Agricultural University; CHEN, LUO - Huazhong Agricultural University; ZHANG, QINGHUA - Huazhong Agricultural University; WANG, MAOJUN - Huazhong Agricultural University; MANSOOR, SHAHID - National Institute Of Biotechnology And Genetic Engineering (NIBGE); ZHANG, XIANLONG - Huazhong Agricultural University; JIN, SHUANGXIA - Huazhong Agricultural University

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/25/2019
Publication Date: 11/1/2019
Citation: Li, J., Hull, J.J., Liang, S., Wang, Q., Chen, L., Zhang, Q., Wang, M., Mansoor, S., Zhang, X., Jin, S. 2019. Genome-wide analysis of cotton miRNAs during whitefly infestation offers new insights into plant-herbivore interaction. International Journal of Molecular Sciences. 20:5357.

Interpretive Summary: Cotton is a major fiber and oil-yielding crop of great economic importance that suffers significant declines in production when attacked by insect herbivores such as whiteflies. Consequently, the genetics underlying cotton defense responses to insect herbivory are of extreme interest. To begin to examine the mechanisms driving the genetic component of the cotton defense pathway, this study used RNA sequencing datasets generated in a previous study that identified two cotton cultivars that exhibited high susceptibility and resistance to whitefly infestation. A number of differences were observed in the sequencing data between the two cultivars with many genetic elements essential to regulating the plant’s stress response differentially expressed in the resistant cultivar. Cotton plants in which a subset of these elements had been genetically disrupted had lowered levels of whitefly infestation and exhibited a shift in the levels of plant signaling hormones. These results offer new insights into how cotton deal with pest infestation and provide specific avenues for future breeding programs to select for resistant cultivars.

Technical Abstract: Although the regulatory function of miRNAs and their targets have been characterized in model plants, a possible underlying role in the cotton response to herbivore infestation has not been determined. To investigate this, we performed small RNA and degradome sequencing between resistant and susceptible cotton cultivar following infestation with the generalist herbivore whitefly. In total, the 260 miRNA families and 241 targets were identified. Quantitative-PCR analysis revealed that several miRNAs and their corresponding targets exhibited dynamic spatio-temporal expression patterns. Moreover, 17 miRNA precursors were generated from 29 long intergenic non-coding RNA (lincRNA) transcripts. The genome-wide analysis also led to the identification of 85 phased small interfering RNA (phasiRNA) loci. Among these, nine PHAS genes were triggered by miR167, miR390, miR482a, and two novel miRNAs, including those encoding a leucine-rich repeat (LRR) disease resistance protein, an auxin response factor (ARF) and MYB transcription factors. Through combined modeling and experimental data, we explored and expanded the miR390-tasiARF cascade during the cotton response to whitefly. Virus-induced gene silencing (VIGS) of ARF8 from miR390 target in whitefly-resistant cotton plants increased auxin and jasmonic acid (JA) accumulation, resulting in increased tolerance to whitefly infestation. These results highlight the provides a useful transcriptomic resource for plant-herbivore interaction.