Transcriptomics and Alternative Splicing Analyses Reveal Large Differences between Maize Lines B73 and Mo17 in Response to Aphid Rhopalosiphum padi Infestation.

Juan Song,Hui Liu,Yuxing Xu,Chunxia Zhao,Christian Hettenhausen,Jianqiang Wu,Huifu Zhuang,Jing Li,Jinfeng Qi,Shibo Wu

doi:10.3389/fpls.2017.01738

Abstract

Maize (Zea mays L.) is a staple crop worldwide with extensive genetic variations. Various insects attack maize plants causing large yield loss. Here, we investigated the responses of maize B73, a susceptible line, and Mo17, a resistant line, to the aphid Rhopalosiphum padi on metabolite and transcriptome levels. R. padi feeding had no effect on the levels of the defensive metabolites benzoxazinoids (Bxs) in either line, and Mo17 contained substantially greater levels of Bxs than did B73. Profiling of the differentially expressed genes revealed that B73 and Mo17 responded to R. padi infestation specifically, and importantly, these two lines showed large gene expression differences even without R. padi herbivory. Correlation analysis identified four transcription factors (TFs) that might account for the high Bx levels in Mo17. Similarly, genome-wide alternative splicing (AS) analyses indicated that both B73 and Mo17 had temporally specific responses to R. padi infestation, and these two lines also exhibited large differences of AS regulation under normal condition, and 340 genes, including 10 TFs, were constantly differentially spliced. This study provides large-scale resource datasets for further studies on the mechanisms underlying maize-aphid interactions, and highlights the phenotypic divergence in defense against aphids among maize varieties.

Highlights

Aphids (Hemiptera: Aphididae) are the most common phloemfeeding pests worldwide
Bx levels are negatively correlated with the growth of the grain aphid Sitobion avenae and R. padi (Thackray et al, 1990), supplementation of Bxs to artificial diet increased the mortality of the greenbug Schizaphis graminum (Argandona et al, 1983), and Bxs are important for the defense against the European Corn Borer Ostrinia nubilalis (Niemeyer, 2009)
Our detailed analyses in control and R. padi-induced B73 and Mo17 indicate that Bx biosynthesisrelated genes and Bx accumulation are not regulated by R. padi feeding

Summary

Introduction

Aphids (Hemiptera: Aphididae) are the most common phloemfeeding pests worldwide. They are devastating to host plants, including crops, due to their capability of very rapid population growth, deprivation of host photosynthates (carbon) and amino acids (nitrogen), reducing photosynthesis, and transmitting viruses (Hales et al, 1997; Smith and Boyko, 2007). Benzoxazinoids (Bxs), known as cyclic hydroxamic acids, are important direct defense metabolites in certain poaceous plants and were first reported in maize and wheat (Triticum aestivum L.) (Wahlroos and Virtanen, 1959). Using maize plants having a mutation in the Bx biosynthesis gene BENZOXAZINELESS1 (BX1), Ahmad et al (2011) demonstrated that Bxs are very important metabolites in maize defense against R. maidis. A genetic study further pointed to the toxicity of HDMBOA-Glc (2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3one glucoside) to R. maidis and the callose inducibility of DIMBOA-Glc (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside) (Meihls et al, 2013)

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Results

Conclusion