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Using RNA-Seq to Characterize Responses to 4-Hydroxyphenylpyruvate Dioxygenase (HPPD) Inhibitor Herbicide Resistance in Waterhemp (Amaranthus Tuberculatus) Daniel R

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Using RNA-Seq to Characterize Responses to 4-Hydroxyphenylpyruvate Dioxygenase (HPPD) Inhibitor Herbicide Resistance in Waterhemp (Amaranthus Tuberculatus) Daniel R Kohlhase et al. BMC Plant Biology (2019) 19:182 https://doi.org/10.1186/s12870-019-1795-x RESEARCH ARTICLE Open Access Using RNA-seq to characterize responses to 4-hydroxyphenylpyruvate dioxygenase (HPPD) inhibitor herbicide resistance in waterhemp (Amaranthus tuberculatus) Daniel R. Kohlhase1, Jamie A. O’Rourke2, Micheal D. K. Owen1* and Michelle A. Graham2* Abstract Background: Waterhemp (Amaranthus tuberculatus (Moq.) J.D. Sauer) is a problem weed commonly found in the Midwestern United States that can cause crippling yield losses for both maize (Zea mays L.) and soybean (Glycine max L. Merr). In 2011, 4-hydroxyphenylpyruvate-dioxygenase (HPPD, EC 1.13.11.27) inhibitor herbicide resistance was first reported in two waterhemp populations. Since the discovery of HPPD-herbicide resistance, studies have identified the mechanism of resistance and described the inheritance of the herbicide resistance. However, no studies have examined genome-wide gene expression changes in response to herbicide treatment in herbicide resistant and susceptible waterhemp. Results: We conducted RNA-sequencing (RNA-seq) analyses of two waterhemp populations (HPPD-herbicide resistant and susceptible), from herbicide-treated and mock-treated leaf samples at three, six, twelve, and twenty-four hours after treatment (HAT). We performed a de novo transcriptome assembly using all sample sequences. Following assessments of our assembly, individual samples were mapped to the de novo transcriptome allowing us to identify transcripts specific to a genotype, herbicide treatment, or time point. Our results indicate that the response of HPPD- herbicide resistant and susceptible waterhemp genotypes to HPPD-inhibiting herbicide is rapid, established as soon as 3 hours after herbicide treatment. Further, there was little overlap in gene expression between resistant and susceptible genotypes, highlighting dynamic differences in response to herbicide treatment. In addition, we used stringent analytical methods to identify candidate single nucleotide polymorphisms (SNPs) that distinguish the resistant and susceptible genotypes. Conclusions: The waterhemp transcriptome, herbicide-responsive genes, and SNPs generated in this study provide valuable tools for future studies by numerous plant science communities. This collection of resources is essential to study and understand herbicide effects on gene expression in resistant and susceptible weeds. Understanding how herbicides impact gene expression could allow us to develop novel approaches for future herbicide development. Additionally, an increased understanding of the prolific traits intrinsic in weed success could lead to crop improvement. Keywords: RNA-seq, de novo transcriptome assembly, herbicide resistance, HPPD, Amaranthus tuberculatus * Correspondence: [email protected]; [email protected] 1Department of Agronomy, Iowa State University, Ames, IA, USA 2U.S. Department of Agriculture (USDA)–Agricultural Research Service (ARS), Corn Insects and Crop Genetics Research Unit, Ames, IA, USA © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kohlhase et al. BMC Plant Biology (2019) 19:182 Page 2 of 19 Background in the resistant population, again attributed to cytochrome Over the past 30 years, waterhemp (Amaranthus tuber- P450 activity. Finding similar resistance mechanisms in culatus (Moq.) J.D. Sauer) has evolved into a major distant populations (Nebraska and Illinois) suggests resist- problem weed species in agricultural production systems ance occurs through spontaneous evolution of standing across the Midwestern United States [1]. If not properly genetic variation [16]. Further, in the HPPD-resistant pop- managed, fields infested with waterhemp can suffer yield ulations examined thus far [17–19], resistance is poly- losses up to 74% in maize (Zea mays L.) and 56% in soy- genic, making identification of causal genes more difficult. bean (Glycine max (L.) Merr.) [2, 3]. Waterhemp is na- None of these studies examined genome wide expression tive to the Midwestern United States and is dioecious; changes in response to mesotrione in resistant and sus- the male and female reproductive structures are on ceptible waterhemp populations. Characterizing gene ex- separate plants. As a dioecious species, waterhemp is an pression differences in HPPD-resistant and susceptible obligatory outcrosser, resulting in high levels of genetic waterhemp populations at time points well before meta- recombination and variability. Obligatory outcrossing bolic responses are detected could help identify major facilitates the movement of ecologically valuable traits, genes contributing to resistance and may provide insight such as herbicide resistance, among and between water- into managing the evolution of resistance to other herbi- hemp populations. Additional biological traits that con- cides in waterhemp and possibly other weed species. tribute to the weediness of waterhemp include prolific Advances in sequencing technologies have created seed production [4], extended and opportunistic germin- opportunities to study the genomics of non-model or- ation [5], and rapid growth rate [6]. ganisms [20]. Due to a lack of weed-related genomic Herbicides are currently the most important tool in resources, Lee et al. [20] sampled 43 million base pairs weed management for most crop production systems in of the waterhemp genome using 454 pyrosequencing many parts of the world [7]. A major concern of modern (Roche Sequencing, Pleasanton, CA, USA). While this weed management is evolved resistance to herbicides. sequencing approach covered less than 10% of the One of the first documented cases of evolved herbicide waterhemp genome, it demonstrated that cutting-edge resistance in weeds was reported in 1970 and since then, sequencing technology could be applied to weed species. the number of unique cases (an individual species x Riggins et al. [21] used 454 pyrosequencing to analyze specific herbicide site of action) has grown to 498 glo- the waterhemp transcriptome. To maximize transcrip- bally and continues to increase [8, 9]. tome coverage, the study pooled RNA samples from dif- In 2011, two waterhemp populations with evolved ferent individuals, sexes, tissues, life stages, herbicide resistance to 4-hydroxyphenylpyruvate dioxygenase treatments, and cold stress. These studies contributed to (HPPD, EC 1.13.11.27) inhibiting herbicides, including a better understanding of the waterhemp genome and mesotrione, were discovered in seed maize fields in Iowa provided sequence-based details for key enzymes tar- and Illinois [10, 11]. Mesotrione (2-(4-Mesyl-2-nitroben- geted by herbicides and potentially prone to herbicide zoyl)-1,3-cyclohexanedione, Herbicide Group (HG) 27) resistance evolution [21]. However, the experimental de- is a selective herbicide that is commonly used for broad- signs and sequencing platforms used in these studies leaf weed control in maize [12]. HPPD converts made it impossible to identify the genes and gene 4-hydroxyphenylpyruvate (4-HPP) to homogentisate networks that regulate susceptibility, tolerance and re- (2,5-dihydroxyphenylacetate; HGA), which is an import- sistance to herbicides. Since these initial studies, ant precursor in carotenoid biosynthesis. The herbicidal RNA-sequencing (RNA-seq) has become the standard activity of mesotrione is characterized by the bleaching method for transcriptome analyses for species lacking of new tissue followed by tissue necrosis. While the genomic resources. resistance mechanisms in the Iowa population have not The increasing prominence of waterhemp as an econom- been determined, in the Illinois population, herbicide re- ically important and ubiquitous weed in the Midwestern sistance was conferred by the metabolism of mesotrione United States and the demonstrated ability to evolve resist- to non-herbicidal metabolites, reportedly attributable to ance to herbicides makes this species an important model increased cytochrome P450 monooxygenase (CYP P450, for studying herbicide resistance evolution in weeds. Here EC 1.14.14.1) activity [13]. In 2017, mesotrione resist- we report on the sequencing of the waterhemp transcrip- ance was confirmed in two waterhemp populations from tome using high throughput RNA-seq technology. This Nebraska (Columbus, NE, [14] and Tarnov, NE, [15]). In study identifies the genes and gene networks responding to the Tarnov population, which was used in this study, the HPPD-inhibiting herbicide mesotrione in susceptible Kaundun et al. [15] found the HPPD gene had no target and resistant waterhemp genotypes over a 24-h exposure site mutations associated with mesotrione resistance, time course. In addition, our study provides a publicly nor was the HPPD gene duplicated or overexpressed. available sequence-based platform for the weed science However, they observed increased mesotrione metabolism community to study this agronomically important weed. Kohlhase et al. BMC Plant Biology (2019) 19:182 Page 3 of 19 Methods
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