INTRODUCTION
Phosphorus (P) is essential for plant growth and development. Low P-availability limits plant growth in most soils because soluble, plant-available inorganic phosphate (Pi) readily forms insoluble complexes with Fe3+ and Al3+ in acidic soils and with Ca2+ in alkaline soils (Hinsinger, 2001; Bertrand et al., 2003). Plants have evolved a variety of developmental, physiological, molecular, and symbiotic strategies to optimize acquisition and utilization of P for growth (Lambers et al., 2011; O’Rourke et al., 2013; Lambers et al., 2015a). Traits associated with adaptation and acclimation to P-limitation include: remodeling of root architecture and development of more and longer root hairs and lateral roots (Lynch, 2011; Lambers et al., 2015b); increased root to shoot ratio (Lynch, 1995); induction of phosphate scavenging and recycling enzymes (Ding et al., 2016); release of carboxylates (Tomasi et al., 2009); P homeostasis by adjustment of major P-pools (Veneklaas et al., 2012); and engagement of specific signal transduction pathways and transcriptional regulatory networks (Misson et al., 2005; Morcuende et al., 2007; Secco et al., 2013). Qualitative and quantitative differences in P-strategies exist between and within species (Lambers et al., 2015b; Pang et al., 2018). Therefore, in order to optimize P efficiency (uptake and utilization) in specific crop species, it is important to investigate the responses and adaptations to P-limitation and the underlying mechanisms in that species and the natural variation that is available for breeding.
Switchgrass, native to the North American tallgrass prairies, is a perennial plant with water-efficient C4 photosynthesis that was targeted for development as a bioenergy crop (Casler et al., 2011; Meyer et al., 2014). Switchgrass exhibits high biomass production potential, relatively low input requirements, and is adapted to much of the eastern half of the USA, including areas considered marginal for food-crop production (Casler et al., 2011; Gopalakrishnan et al., 2011; King et al., 2013; Meyer et al., 2014). Some research suggests that biomass-to-energy schemes using marginal lands would provide substantial ecosystem services, particularly in terms of carbon sequestration and other environmental benefits (Bhardwaj et al., 2011; Gelfand et al., 2013). Data on switchgrass production on marginal sites are limited. Previous research has shown that switchgrass biomass yields respond to nitrogen fertilizer rates of up to 168 kg ha-1, depending on ecotype and location (Sanderson et al., 1999; Muir et al., 2001; Guretzky et al., 2011). In soils with low plant-available P, application of 45 kg P ha-1 increased biomass yield by up to 17% (Kering et al., 2012).
Switchgrass has been subjected to a genome sequencing effort (Casler et al., 2011) as well as transcriptome analyses, using Expressed Sequence Tags (ESTs), Affymetrix oligonucleotides arrays, and RNA-seq (Sharma et al., 2012; Zhang et al., 2013; Meyer et al., 2014; Yang et al., 2016). Transcriptome analyses have identified thousands of genes associated with drought stress (Meyer et al., 2014) and leaf senescence in switchgrass (Yang et al., 2016), but transcriptional responses to P limitation have not been reported. Likewise, metabolic responses of switchgrass to P deficiency remain unknown, although advanced technologies are available (Sanchez et al., 2008; Luo et al., 2017). We characterized the physiological and developmental responses of switchgrass to P-limitation and explored underlying transcriptional and metabolic responses in shoots and roots. Results and insights are presented here.