Characterization of the rice NLA family reveals a key role for OsNLA1 in phosphate homeostasis

Rice, Dec 2017

Background Phosphate (Pi), an essential mineral nutrient for plant development and reproduction, is one of the main components of fertilizers in modern agriculture. Previous research demonstrated that AtNLA1 mediates ubiquitination of Pi transporters in the plasma membrane and triggers their endocytosis and degradation in Arabidopsis. In this study, we researched the function of NLA homologous proteins in Pi homeostasis in rice. Findings Two OsNLA homologs from rice (Oryza sativa L.) were identified by bioinformatics and phylogenetic analysis and designated OsNLA1 and OsNLA2. The OsNLA1 clustered with Arabidopsis AtNLA1, was expressed higher than OsNLA2 and was transcriptionally repressed under Pi-deficient condition. Loss-of-function of OsNLA1 caused P overaccumulation and growth inhibitions in both root and shoot under Pi-sufficient condition. Furthermore, mutation of OsNLA1 affected expression of Pi tranporters and root hair development under Pi-sufficient and/or Pi-deficient conditions. Conclusions OsNLA1 plays a key role in maintaining phosphate homeostasis in rice.

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Characterization of the rice NLA family reveals a key role for OsNLA1 in phosphate homeostasis

Yang et al. Rice Characterization of the rice NLA family reveals a key role for OsNLA1 in phosphate homeostasis Jian Yang 0 Lan Wang 0 2 Chuanzao Mao 1 Honghui Lin 0 0 Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Science, Sichuan University , Chengdu 610064 , China 1 State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University , Hangzhou 310058 , China 2 Biogas Institute of Ministry of Agriculture , Chengdu 610041 , China Background: Phosphate (Pi), an essential mineral nutrient for plant development and reproduction, is one of the main components of fertilizers in modern agriculture. Previous research demonstrated that AtNLA1 mediates ubiquitination of Pi transporters in the plasma membrane and triggers their endocytosis and degradation in Arabidopsis. In this study, we researched the function of NLA homologous proteins in Pi homeostasis in rice. Findings: Two OsNLA homologs from rice (Oryza sativa L.) were identified by bioinformatics and phylogenetic analysis and designated OsNLA1 and OsNLA2. The OsNLA1 clustered with Arabidopsis AtNLA1, was expressed higher than OsNLA2 and was transcriptionally repressed under Pi-deficient condition. Loss-of-function of OsNLA1 caused P overaccumulation and growth inhibitions in both root and shoot under Pi-sufficient condition. Furthermore, mutation of OsNLA1 affected expression of Pi tranporters and root hair development under Pi-sufficient and/or Pi-deficient conditions. Conclusions: OsNLA1 plays a key role in maintaining phosphate homeostasis in rice. Rice; Phosphate; OsNLA1; Pi-homeostasis Findings Phosphorus (P) is a mineral nutrient essential for plant development and reproduction, and is integral to several macromolecules such as phospholipids and nucleic acids. Despite the indispensable role of P for plants, levels of phosphate (orthophosphate; Pi), the only form of P that can be taken up by plants, are commonly limited because of chemical fixation and microbial activity (Raghothama, 1999) . To cope with suboptimal Pi conditions, plants have developed a series of adaptive responses, such as induction of Pi transporters and modification of root system architecture (Raghothama, 1999; Lin et al., 2009; Wu et al., 2013) . Plant uptake of Pi is largely mediated by plasma membrane -localized Pi transporters belonging to the PHOSPHATE TRANSPORTER1 (PT) symporter family. Thirteen PT genes have been identified in rice (Oryza sativa) and nine in Arabidopsis thaliana (Goff et al., 2002; Karthikeyan et al., 2002) . OsPTs differ in tissue expression patterns and affinities for Pi, resulting in diverse functions in plants. For instance, the high-affinity Pi transporter OsPT8 is universally expressed in rice, and is responsible for half of its Pi uptake (Chen et al., 2011; Jia et al., 2011) . Although most OsPTs in rice are induced at the transcriptional level by Pi starvation or mycorrhizal symbiosis (Yang et al., 2012; Secco et al., 2013) , post-transcriptional regulating of OsPT family proteins is also important to their activities (Gonzalez et al., 2005; Bayle et al., 2011; Chen et al., 2011; Chen et al., 2015) . NITROGEN LIMITATION ADAPTATION (NLA), designated AtNLA1 in this study, was first identified as a positive regulator for the adaptability of Arabidopsis to nitrogen limitation (Peng et al., 2007) , and later analysis of Pi concentration revealed that the early senescence phenotype of atnla mutant plants was due to Pi toxicity (Kant et al., 2011) . In Arabidopsis, AtNLA1 can interact with AtPTs members via its SPX domain, and mediate ubiquitination of AtPTs in the plasma membrane and trigger their endocytosis and degradation (Lin et al., 2013; Park et al., 2014) . Recently, two research groups separately reported roles of OsNLA1 in mantaining Pi homeostasis in rice (Yue et al., 2017; Zhong et al., 2017) . Yue et al., (2017) additionally reported OsNLA1 functioned as a ubiquitin ligase to degrade Pi transporters in rice, with a similar function of AtNLA1 in Arabidopsis.. In this study, we were interested in the phylogenetic relationship of the NLA family and expression of OsPTs and root hair development in osnla1 mutant. An unrooted phylogenetic analysis of the NLA family proteins with four monocots (B. distachyon, S. bicolor, S. italica and rice) and five dicots (grapevine, soybean, apple, M. truncatula and Arabidopsis), revealed the presence of two distinct clades. Although all plants had proteins belonging to clade I, in which AtNLA1 involved in regulating Pi homeostasis was present (Kant et al., 2011) , all monocots and only some dicots had NLA members belonging to clade II (Fig. 1a). This suggested that NLA members of clade I conservatively functioned in maintaining Pi homeostasis among different plant species. Quantitative reverse-transcription PCR (qRT-PCR) was performed on different tissues for rice plants grown in nutrient solutions under Pi (...truncated)


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Jian Yang, Lan Wang, Chuanzao Mao, Honghui Lin. Characterization of the rice NLA family reveals a key role for OsNLA1 in phosphate homeostasis, Rice, 2017, pp. 52, Volume 10, Issue 1, DOI: 10.1186/s12284-017-0193-y