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Induced Transcriptional Profiling of Phenylpropanoid Pathway Genes

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Induced Transcriptional Profiling of Phenylpropanoid Pathway Genes Ali and McNear BMC Plant Biology 2014, 14:84 http://www.biomedcentral.com/1471-2229/14/84 RESEARCH ARTICLE Open Access Induced transcriptional profiling of phenylpropanoid pathway genes increased flavonoid and lignin content in Arabidopsis leaves in response to microbial products Mohammad Babar Ali* and David H McNear Jr Abstract Background: The production and use of biologically derived soil additives is one of the fastest growing sectors of the fertilizer industry. These products have been shown to improve crop yields while at the same time reducing fertilizer inputs to and nutrient loss from cropland. The mechanisms driving the changes in primary productivity and soil processes are poorly understood and little is known about changes in secondary productivity associated with the use of microbial products. Here we investigate secondary metabolic responses to a biologically derived soil additive by monitoring changes in the phenlypropanoid (PP) pathway in Arabidopsis thaliana. Results: This study was designed to test the influence of one of these products (Soil Builder™-AF, SB) on secondary metabolism after being applied at different times. One time (TI) application of SB to Arabidopsis increased the accumulation of flavonoids compared to multiple (TII) applications of the same products. Fourteen phenolic compounds including flavonols and anothocyanins were identified by mass spectrometry. Kaempferol-3,7-O-bis-α- L-rhamnoside and quercetin 3,7-dirhamnoside, the major compounds, increased 3-fold and 4-fold, respectively compared to control in the TI treatment. The most abundant anthocyanin was cyanidin 3-rhamnoglucoside, which increased 3-fold and 2-fold in TI compared to the control and TII, respectively. Simultaneously, the expression of genes coding for key enzymes in the PP pathway (phenylalanine ammonia lyase, cinnamate 4-hydroxylase, chalcone synthase, flavonoid-3′-O-hydroxylase, flavonol synthase1 and dihydroflavonol-4-reductase) and regulatory genes (production of anthocyanin pigment2, MYB12, MYB113, MYB114, EGL3, and TT8) were up-regulated in both treatments (TI and TII). Furthermore, application of TI and TII induced expression of the lignin pathway genes (hydroxyl cinamyl transferase, caffeyl-CoA O-methyl transferase, cinnamyl alcohol dehydrogenase, cinnamyl-CoA reductase,secondary wall-associated NAC domain protein1, MYB58 and MYB63 resulting in higher accumulation of lignin content compared to the control. Conclusions: These results indicate that the additions of microbially based soil additives have a perceptible influence on phenylpropanoid pathway gene regulation and its production of secondary metabolites. These findings open an avenue of research to investigate the mode of action of microbially-based soil additives which may assist in the sustainable production of food, feed, fuel and fiber. Keywords: Arabidopsis, Metabolites, Microbes, Transcriptional profiling, Plant Growth Promoting Rhizobacteria, Soil Builder * Correspondence: [email protected] Department of Plant and Soil Sciences, Rhizosphere Science Laboratory, University of Kentucky, Lexington, KY 40546, USA © 2014 Ali and McNear; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Ali and McNear BMC Plant Biology 2014, 14:84 Page 2 of 14 http://www.biomedcentral.com/1471-2229/14/84 Background to help plants fight microbial diseases [14]. In addition, One of major challenges in the 21st century is the sus- several studies have examined how the PP and defense re- tainable production of food, fuel and fiber crops with en- lated pathways are regulated by interactions between soil hanced functional and nutritive value (e.g. flavonoids microorganisms and plant roots [15-18]. The genes in- and anthocyanins) to meet the demands of an ever- volved in PP pathway such as chalcone synthase (CHS), increasing global population [1,2]. To meet this demand chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), requires the development of alternative more sustainable flavonoid 3’-hydroxylase (F3’H), and flavonol synthase1 methods for the production and enhancement of value (FLS1) play important roles in the production of secon- added agricultural commodities in a way that will have dary metabolites, while dihydroflavonol 4-reductase (DFR), minimal impact on the ecosystem. Current agricultural and leucoanthocyanidin dioxygenase (LDOX) are involved practices are largely based on the use of chemical fertil- in the production of colored anthocyanidins (Additional izers and synthetic pesticides for improved crop growth file 1). After production, these products are further mo- and yield. However, our dependence and overuse of these dified by glycosylation, acylation, and methylation in a fertilizers has resulted in contamination of soil, ground and complex process that changes their stability, solubility, or surface waters. Increasing demand for healthier and more localization, and thereby the biological properties of the nutrient-dense foods by more health-conscious consumers conjugated molecules [19]. and an improved environmental awareness has resulted in The transcription factors regulating the expression of an increased interest in and a rapid change towards eco- these structural genes have been well characterized in friendly sustainable agricultural farming systems. plant species including Arabidopsis [20]. MYB11, MYB12, One component of this new sustainable production and MYB111 encode three functionally redundant MYBs system is the use of microbe-based fertilizers (i.e. biosti- regulating the expression of several ‘early’ flavonoid bio- mulants) containing potential beneficial strains of micro- synthetic genes [21]. On the other hand, TFs such as PAP1, organism and their metabolites many of which have an PAP2, GL3, TT8 and TTG1 which are components of the important role in conditioning the rhizosphere for im- MYB/bHLH/WDR (MBW) transcriptional complexes medi- proved plant growth and nutrient use efficiency [3,4]. ate the ‘late’ anthocyanin biosynthesis genes [21,22]. The Since the 1970’s we have been cognizant of the potential lignin biosynthesis pathway is well-characterized and plays benefits on plant growth of specialized plant growth pro- an important role in plant growth, development, increase moting rhizobacteria (PGPR) [5]. There have been many cell wall integrity, facilitating water transport and providing reports on improvements in plant defense, health and resistance against pathogen [23-25]. The genes which are growth, resistance to pathogens, enhanced salt tolerance, involved in lignin biosynthesis are largely regulated at the and improved nutrient uptake in response to PGPR [6,7] transcription level and lignin-specific transcription factor that could have led to the development of novel agricul- MYB58, MYB63 and SND1 can induce the biosynthetic tural applications. In spite of all these advantages, the pathways for the synthesis of lignin [26,27]. use of microbial-based products has not been effectively To date there is little research aimed at understanding exploited at larger scales to improve plant yields and most the influence of microbial products on plant secondary certainly not as a means to selectively enhance gene ex- metabolism making it difficult to assess a potential func- pression and production of beneficial secondary metabo- tional relationship(s). Understanding how phenylpropa- lite in crops. noid metabolism changes in response to microbes or Phenylpropanoids are a large group of polyphenolic microbial-based products will help to improve our funda- compounds that comprise an important class of second- mental understanding of plant biology, and would be useful ary metabolites such as flavonoids, anthocyanin and lig- for the development of natural products aimed at improv- nin in plants [8]. Phenylpropanoids have important ing crop yield and quality. Preliminary analysis of the prod- functions in flower coloration, pollinator attraction, pro- uct composition shows that it is composed of PGPR related tection from ultraviolet (UV) light, as signaling mole- bacteria and use of the product can result in plant growth cules between plants and microbes, and as antioxidants promotion [28,29]. We hypothesized that microbial-based [9]. Additionally, when consumed by humans phenylpro- products, known to improve plant growth and nutrient panoids offer a myriad of health benefits [10,11]. There uptake, can induce the PP pathway and lignin pathway have been many studies on the biosynthesis of flavonols in Arabidopsis. Therefore, this study was designed to and the PP pathway in general via metabolic engineering evaluate how application and the timing of application targeting important agronomic traits such as the produc- (single and multiple times) influence the PP pathway in tion of novel colors and color patterns in ornamentals Arabidopsis. Quantitative real-time PCR (qRT-PCR) was [8,12]. Many phenylpropanoids act as inducers of plant- used in this study for transcriptional profiling of flavonoid microbe symbioses [13], whereas others exhibit broad- and lignin pathway genes, and high performance liquid spectrum antimicrobial activity and are therefore believed chromatography (HPLC) and liquid chromatography- Ali and McNear BMC Plant Biology 2014, 14:84 Page 3 of 14 http://www.biomedcentral.com/1471-2229/14/84
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