Physiological responses and transcriptomic changes reveal the mechanisms underlying adaptation of Stylosanthes guianensis to phosphorus deficiency

Abstract

Background Phosphorus (P) is an essential macronutrient for plant growth that participates in a series of biological processes. Thus, P deficiency limits crop growth and yield. Although Stylosanthes guianensis (stylo) is an important tropical legume that displays adaptation to low phosphate (Pi) availability, its adaptive mechanisms remain largely unknown. Results In this study, differences in low-P stress tolerance were investigated using two stylo cultivars (‘RY2’ and ‘RY5’) that were grown in hydroponics. Results showed that cultivar RY2 was better adapted to Pi starvation than RY5, as reflected by lower values of relative decrease rates of growth parameters than RY5 at low-P stress, especially for the reduction of shoot and root dry weight. Furthermore, RY2 exhibited higher P acquisition efficiency than RY5 under the same P treatment, although P utilization efficiency was similar between the two cultivars. In addition, better root growth performance and higher leaf and root APase activities were observed with RY2 compared to RY5. Subsequent RNA-seq analysis revealed 8,348 genes that were differentially expressed under P deficient and sufficient conditions in RY2 roots, with many Pi starvation regulated genes associated with P metabolic process, protein modification process, transport and other metabolic processes. A group of differentially expressed genes (DEGs) involved in Pi uptake and Pi homeostasis were identified, such as genes encoding Pi transporter (PT), purple acid phosphatase (PAP), and multidrug and toxin extrusion (MATE). Furthermore, a variety of genes related to transcription factors and regulators involved in Pi signaling, including genes belonging to the PHOSPHATE STARVATION RESPONSE 1-like (PHR1), WRKY and the SYG1/PHO81/XPR1 (SPX) domain, were also regulated by P deficiency in stylo roots. Conclusions This study reveals the possible mechanisms underlying the adaptation of stylo to P deficiency. The low-P tolerance in stylo is probably manifested through regulation of root growth, Pi acquisition and cellular Pi homeostasis as well as Pi signaling pathway. The identified genes involved in low-P tolerance can be potentially used to design the breeding strategy for developing P-efficient stylo cultivars to grow on acid soils in the tropics.

Integrated multi-omics reveals the molecular mechanisms underlying efficient phosphorus use under phosphate deficiency in elephant grass (Pennisetum purpureum)

“…The total P concentration was determined by phosphorusmolybdate blue color reaction, and the optical density at 700 nm (OD 700 ) value of reaction products was measured by spectrophotometry (Bio-Rad, CA, USA), as described by Murphy and Riley (1962). Finally, P content and P utilization efficiency were calculated depending on the dry weight and total P concentration of plant samples, as described previously (Chen et al, 2021). After 10 days of Pi treatment, mixed leaves (including upper, middle, and lower leaves) and whole roots were harvested for APase activity, transcriptome, and metabolome analyses, with each treatment including three biological replicates (four seedlings from each treatment were combined to form one biological replicate).…”

“…PAPs are a unique class of APases, the most well-studied gene family contributing to Pi acquisition (Tran et al, 2010). Previous studies reported that 10 out of 26 OsPAP genes in O. sativa, 11 out of 33 ZmPAP genes in Z. mays, 23 out of 35 GmPAP genes in G. max, 20 out of 25 SlPAP genes in Solanum lycopersicum, and 21 out of 23 SgPAP genes in Stylosanthes guianensis were upregulated upon low-Pi stress (Zhang et al, 2011;Li et al, 2012;Gonza ́lez-Muñoz et al, 2015;Srivastava et al, 2020;Chen et al, 2021). Consistently, we found that 18 and 11 out of 48 PAP unigenes were up-regulated in leaves and roots, respectively, under Pi deficiency in elephant grass (Figure 3B).…”

SgNramp1, a plasma membrane-localized transporter, involves in manganese uptake in Stylosanthes guianensis

“…Five Nramp genes were isolated from the previously reported transcriptomic data in stylo ( Jiang et al., 2018 ; Jia et al., 2020 ; Chen et al., 2021 ). The full length of each Nramp was amplified from the cDNA library stock of stylo roots ( Song et al., 2022 ).…”

“…Stylo is an acid soil adapted, pioneer forage legume, which is widely used for multipurpose including land reclamation and restoration, soil quality improvement, and fodder for farm animals ( Tang et al., 2009 ; Marques et al., 2018 ; Guo et al., 2019 ). Stylo displays superior level of tolerance to nutrient and metal stresses that are common in acid soils of the tropics, including phosphorus (P) deficiency, excess Mn stress, and Al toxicity ( Sun et al., 2014 ; Chen et al., 2015 ; Chen et al., 2021 ). Considering the key role of Nramp in metal ion uptake and homeostasis, this study aimed to determine the responses of Nramp genes to metal stress and investigate its roles in metal transport activity.…”

Improving phosphorus acquisition efficiency through modification of root growth responses to phosphate starvation in legumes

“…PAE is regarded as the ability of plants to acquire soil P by roots, while PUE is thought to be the ability of plants to generate biomass or yield using the acquired P (Wang et al, 2010;Han et al, 2022). In P-limited soils, enhancement of PAE is a key strategy that has received considerable attention with a focus on optimizing root traits including: (1) root growth responses that involve changes in root morphology (e.g., primary root, lateral roots, root hairs, and cluster roots) and root architecture, contributing to acquire more P from soils by extension of root system (Lynch, 2011;Li et al, 2016;Zhang et al, 2018;Chen et al, 2021;Liu, 2021;Lynch et al, 2022); (2) coordination of physiological and biochemical alterations of root traits, such as exudation of protons, organic acids and phosphatases into the rhizosphere, facilitating P mobilization from the unavailable P in the rhizosphere (Pang et al, 2018a;Robles-Aguilar et al, 2019;Wen et al, 2019); (3) establishing symbiotic interactions with beneficial microbes (e.g., Pi-solubilizing bacteria) or arbuscular mycorrhizal fungi (AMF) to improve PAE by solubilizing and foraging P (Khan et al, 2014;Campos et al, 2018). Thus, genetic modification of root system traits can be an effective strategy for improving crop varieties with low P tolerance and high PAE.…”