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New insights into plant nutrient signaling and adaptation to fluctuating environments
Journal of Genetics and Genomics 43 (2016) 621e622
Contents lists available at ScienceDirect
Journal of Genetics and Genomics Journal homepage: www.journals.elsevier.com/journal-of-geneticsand-genomics/
Editorial
New insights into plant nutrient signaling and adaptation to fluctuating environments Over the past 50 years, the Green Revolution and exploitation of heterosis have allowed cereal grain yield to keep pace with worldwide population growth. Unfortunately, plant growth and crop productivity are heavily dependent on the application of synthetic fertilizers. In the next 50 years, global population is projected to be 50% larger than at present and global food demand is projected to double (Tilman et al., 2002). Further increases in fertilizer supplies are unlikely to be effective in improving grain yield because of diminishing returns and their deleterious impact on public health and environmental problems. Therefore, increasing nutrient-use efficiency is crucial for development of sustainable agriculture. Plant root systems acquire nutrients (e.g., nitrogen, phosphate, potassium and sulfur) through uptake from the soils, whereas the natural supply of soil nutrient content varies in different soil conditions, such as aerobic soils, flooded wetland and acidic soils, which is frequently limiting for plant growth and crop yield. Thus, as sessile organisms, plants have evolved a number of developmental plasticity and metabolic responses to adapt both the internal nutrient status in planta and the external soil nutrient availability. Moreover, the roots not only can locally sense and respond to changes in nutrient availability in soils, but also can communicate with the shoots, which then transfers long-distance signals back to the roots to facilitate nutrient uptake via the regulation of transporter activity and root architectures. Recently, major advances have been made in identifying the key components that impact both plant development and metabolism in response to nutrient availability and in understanding of coordinated regulation between plant growth and nutrient acquisition. This special issue contains one perspective, one review, three original research articles and one letter to the editor, which reveal the genetic control of plant nutrient assimilation and use efficiency. The aim is to understand the complex networks and integrative signaling pathways which are prerequisite for developmental plasticity and environmental adaptability in model and crop plants. Nitrogen is a major limiting nutrient for plant growth and crop productivity. Root systems absorb and assimilate nitrogen in many different forms, such as nitrate, ammonium, amino acids and other nitrogen-containing substances. Nitrate is the main source of inorganic nitrogen for plants in aerobic soil conditions, whereas ammonium is the major form of inorganic nitrogen in flooded wetland or acidic soil conditions. For most plants, a small part of nitrate taken up by nitrate transporters (NRTs) in the roots can be assimilated into ammonium and further to amino acids in the roots, but the larger part is translocated to the shoots, where it is reduced to nitrite by nitrate reductase (NR) and further to ammonium by nitrite
reductase (NiR). For rice, ammonium is likely taken up by ammonium transporters (AMTs) and assimilated by glutamine synthetase (GS) and glutamine-2-oxoglutarate amino-transferase (GOGAT) within the organ of root systems. The rice genome encodes at least 10 putative AMT-like transporters, which group into four subfamilies (OsAMT1eOsAMT4), and the three members of the rice OsAMT1 gene family functionally complement the growth of a yeast mutant deficient in ammonium uptake. The transgenic rice plants overexpressing OsAMT1.1 had a higher ammonium content in shoots and roots than non-transgenic wild-type plants. Higher expression of OsAMT1.1 also enhanced overall plant growth under low ammonium conditions, but resulted in worse growth under high ammonium conditions. Although OsAMT1.1 is constitutively expressed in both roots and shoots, the temporal and spatial regulation and function of OsAMT1.1 in maintaining nitrogen homeostasis still remain unclear. Li et al. showed that the expression of OsAMT1.1 was rapidly induced by ammonium in both shoots and roots, but potassium starvation suppressed the expression of OsAMT1.1 in both shoots and roots. To investigate whether OsAMT1.1 is involved in the interaction between nitrogen and potassium in the uptake and assimilation, Li et al. generated the rice osamt1.1 null mutants using CRISPR/Cas9 technology. Compared to wild-type plants, the osamt1.1 mutants had decreased uptake capacity of potassium under low ammonium conditions, but had a higher potassium content in shoots and roots at limited potassium supply when ammonium was replete. These genetic evidences reveal that OsAMT1.1 plays an important role for maintaining the nitrogen and potassium homeostasis in rice (pp. 639e649). Recently, microRNAs (miRNAs) have been identified as the important regulatory factors in controlling nutrient starvation responses. In Arabidopsis, solexa sequencing technology has been used to detect changes in the expression patterns of miRNAs under nitrate-sufficient and nitrate-deficient conditions. The expression of four miRNAs (e.g., miR160) was significantly upregulated under nitrogen starvation conditions. Induced miR160 mediated the cleavage of ARF16 and promoted lateral root production in Arabidopsis. Interestingly, 20 novel miRNAs were identified and nine of them were responsive to nitrate starvation. To date, however, there is few genome-wide studies on rice miRNAs involved in nitrogen starvation responses. Li et al. performed high-throughput small RNA sequencing under different nitrate and ammonium conditions. The deep sequencing results clearly showed that nitrogenregulated expression patterns of miRNAs significantly differentiated between nitrate and ammonium treatments. There are 16 miRNAs induced by nitrate and 11 miRNAs induced by ammonium
http://dx.doi.org/10.1016/j.jgg.2016.11.004 1673-8527/Copyright © 2016, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China. Published by Elsevier Limited and Science Press. All rights reserved.
622
Editorial / Journal of Genetics and Genomics 43 (2016) 621e622
under short-term treatments, and there are 60 differentially expressed miRNAs between nitrate and ammonium under longterm treatments. The expression of OsmiR160 induced by ammonium was higher than that induced by nitrate, whereas miR164 was done in opposite ways. Theses comprehensive expression profiling of miRNAs in response to nitrate and/or ammonium starvation conditions presents an advance in understanding the regulation of different nitrogen signaling and homeostasis mediated by miRNAs (pp. 651e661). Unlike various nitrogen forms, phosphorus (P) forms insoluble compounds in acidic soils, or is unevenly distributed as phosphate (Pi) in alkaline soils. Thus, Pi availability in soils is often a key limiting factor for plant growth in both natural and agricultural systems. To cope with low Pi availability, plants have to reprogram gene expression profile to facilitate Pi acquisition and assimilation. Previous studies have demonstrated that AtPHR1 and OsPHR2 play the important roles in Pi signaling. Recently, crystal structures of SPX protein reveal that SPX domains function as inositol polyphosphate (InsP) sensor. InsP binding allows SPX domains to interact with transcription factors AtPHR1 and OsPHR2, and the SPX-PHR protein complex prevents AtPHR1 and OsPHR2 from binding their target promoters, which in turn regulates Pi homeostasis. In addition, plants evolve a number of developmental responses to adapt both the internal Pi status in planta and the external soil Pi availability, including changes in shoot-root ratio and formation of highly branched root systems, which enhance the exploratory capacity of roots to search for Pi-rich patches present in the soil. Thus, the improvement of root architectures is a major breeding target to enhance Pi assimilation and use efficiency. Gu et al. showed that two maize inbred lines Ye478 and Wu312 exhibited substantial variations with respect to phosphorus-use efficiency (PUE) and root system architecture (RSA). It resulted in the identification of quantitative trait loci (QTLs) presumed to determine PUE in maize. Using 218 recombination inbred lines derived from the cross between Ye478 and Wu312, Gu et al. identified two QTL-clusters Clbin3.04a and Cl-bin3.04b responsible for PUE and RSA. More importantly, combining Cl-bin3.04a and Cl-bin3.04b loci can be effective in simultaneously improving PUE and RSA in both hydroponics and field conditions. This genetic result links RSA to PUE, and provides a new strategy to improve maize PUE through QTL-based selection of root system architectures (pp. 663e672). Sulfur is also an essential plant nutrient, necessary for synthesis of many metabolites which are important for biotic and abiotic interactions of plant growth and food production in terms of both grain yield and grain quality. Inorganic sulfate (SO 4 ) is taken up from the soil by plants via their root system, which is activated by adenylation to adenosine 5'-phosphosulfate (APS) by ATP sulfurylase, and further phosphorylated to 3'-phosphoadenosine-5'phosphosulfate, which is used for sulfation reactions. Cys is the key metabolite in the synthesis of sulfur-containing compounds in plants, while the major pool of sulfur, which is not stored in proteins, is the Cys-containing peptide GSH. Koprivova and Kopriva describe recent progress in dissection of the regulatory network of sulfate uptake and homeostasis by transcriptional and posttranscriptional regulation of sulfur transport, as well as sulfur metabolism and reutilization. The perspective also describes the molecular mechanisms of how plants adapt to changes in sulfur availability, and highlights the genetic approaches to increase sulfur assimilation and use efficiency to improve crop productivity (pp. 623e629). In acidic soils, aluminum (Al) becomes more soluble and ionic Al3þ dramatically inhibits root growth and nutrients uptake, meanwhile, P fixation with Al and Fe oxides results in more severe reduction of Pi availability. Thus, plants have to evolve diverse strategies
to simultaneously cope with Al toxicity and Pi deficiency under acidic soil conditions. Chen and Liao summarize the latest advances in the understanding of the molecular mechanisms for exudation and metabolism of organic acid anions (OAs), such as malate, citrate and oxalate, which are secreted by roots into the rhizosphere to chelate Al3þ and mobilize Pi, thereby serving as a defense weapon for plants against both Al toxicity and Pi deficiency under acidic soil conditions. The exudation of OAs varies widely among various plant species and fluctuating environments, and the transporters (e.g., ALMT and MATE) responsible for OA secretion and metabolic enzymes involved in OA biosynthesis have been functionally characterized in model and crop plants. In addition, the genetic manipulation of OA metabolism and transport provides an effective way to enhance tolerance to high Al3þ and low Pi stresses, suggesting that the application of CRISPR/Cas9 genome editing technology can help to improve crop productivity in acidic soils (pp. 631e638). Unlike other macronutrients, copper (Cu) is an essential micronutrient, but it is also highly toxic to plant growth and development when in excess. Importantly, Cu has been used as a way to increase the efficiency of animal production because of the low Cu content in most sources of feed. Cu in plants is often present in complex forms bound to cysteine-rich proteins and carboxylic and phenolic groups, and its deficiency has been reported in many crops. The previous studies have shown that SBP-domain transcription factor AtSPL7 regulates Cu uptake and relocation in Arabidopsis. Tang et al. identified rice OsSPL9 with sequence homolog to AtSPL7, and generated transgenic rice plants, in which OsSPL9 was constitutively expressed. Compared to wild-type plants, the transgenic rice plants exhibited similar phenotypes with respect to root systems, plant height and grain yield. However, the up-regulation of OsSPL9 promoted the expression of several COPT genes that encode copper transporters, resulting in high-level accumulation of organic copper in grain and improvement in its digestibility, which indicates that genetic manipulation of OsSPL9 and its ortholog represents a new way toward Cu biofortification in rice (pp. 673e676). Improving plant nutrient use efficiency is essential for the development of sustainable agriculture, however, plant nutrient use efficiency is a complex trait determined by QTLs and influenced by fluctuating environments (Liu et al., 2015). These articles included in this special issue have covered several aspects of highly intergraded signaling pathways that control nutrient uptake, metabolism, and associated starvation responses. Further identification of new components that mediate nutrient signaling using genome-wide approaches and understanding of the regulatory networks and crosstalk with other phytohormone signaling pathways will help to improve nutrient use efficiency and crop productivity.
References Liu, Q., Chen, X., Wu, K., Fu, X., 2015. Nitrogen signaling and use efficiency in plants: what's new? Curr. Opin. Plant Biol. 27, 192e198. Tilman, D., Cassman, K.G., Matson, P.A., Naylor, R., Polasky, S., 2002. Agricultural sustainability and intensive production practices. Nature 418, 671e677.
Xiangdong Fu The State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China E-mail address: [email protected]. 11 November 2016 Available online 13 November 2016
Contents lists available at ScienceDirect
Journal of Genetics and Genomics Journal homepage: www.journals.elsevier.com/journal-of-geneticsand-genomics/
Editorial
New insights into plant nutrient signaling and adaptation to fluctuating environments Over the past 50 years, the Green Revolution and exploitation of heterosis have allowed cereal grain yield to keep pace with worldwide population growth. Unfortunately, plant growth and crop productivity are heavily dependent on the application of synthetic fertilizers. In the next 50 years, global population is projected to be 50% larger than at present and global food demand is projected to double (Tilman et al., 2002). Further increases in fertilizer supplies are unlikely to be effective in improving grain yield because of diminishing returns and their deleterious impact on public health and environmental problems. Therefore, increasing nutrient-use efficiency is crucial for development of sustainable agriculture. Plant root systems acquire nutrients (e.g., nitrogen, phosphate, potassium and sulfur) through uptake from the soils, whereas the natural supply of soil nutrient content varies in different soil conditions, such as aerobic soils, flooded wetland and acidic soils, which is frequently limiting for plant growth and crop yield. Thus, as sessile organisms, plants have evolved a number of developmental plasticity and metabolic responses to adapt both the internal nutrient status in planta and the external soil nutrient availability. Moreover, the roots not only can locally sense and respond to changes in nutrient availability in soils, but also can communicate with the shoots, which then transfers long-distance signals back to the roots to facilitate nutrient uptake via the regulation of transporter activity and root architectures. Recently, major advances have been made in identifying the key components that impact both plant development and metabolism in response to nutrient availability and in understanding of coordinated regulation between plant growth and nutrient acquisition. This special issue contains one perspective, one review, three original research articles and one letter to the editor, which reveal the genetic control of plant nutrient assimilation and use efficiency. The aim is to understand the complex networks and integrative signaling pathways which are prerequisite for developmental plasticity and environmental adaptability in model and crop plants. Nitrogen is a major limiting nutrient for plant growth and crop productivity. Root systems absorb and assimilate nitrogen in many different forms, such as nitrate, ammonium, amino acids and other nitrogen-containing substances. Nitrate is the main source of inorganic nitrogen for plants in aerobic soil conditions, whereas ammonium is the major form of inorganic nitrogen in flooded wetland or acidic soil conditions. For most plants, a small part of nitrate taken up by nitrate transporters (NRTs) in the roots can be assimilated into ammonium and further to amino acids in the roots, but the larger part is translocated to the shoots, where it is reduced to nitrite by nitrate reductase (NR) and further to ammonium by nitrite
reductase (NiR). For rice, ammonium is likely taken up by ammonium transporters (AMTs) and assimilated by glutamine synthetase (GS) and glutamine-2-oxoglutarate amino-transferase (GOGAT) within the organ of root systems. The rice genome encodes at least 10 putative AMT-like transporters, which group into four subfamilies (OsAMT1eOsAMT4), and the three members of the rice OsAMT1 gene family functionally complement the growth of a yeast mutant deficient in ammonium uptake. The transgenic rice plants overexpressing OsAMT1.1 had a higher ammonium content in shoots and roots than non-transgenic wild-type plants. Higher expression of OsAMT1.1 also enhanced overall plant growth under low ammonium conditions, but resulted in worse growth under high ammonium conditions. Although OsAMT1.1 is constitutively expressed in both roots and shoots, the temporal and spatial regulation and function of OsAMT1.1 in maintaining nitrogen homeostasis still remain unclear. Li et al. showed that the expression of OsAMT1.1 was rapidly induced by ammonium in both shoots and roots, but potassium starvation suppressed the expression of OsAMT1.1 in both shoots and roots. To investigate whether OsAMT1.1 is involved in the interaction between nitrogen and potassium in the uptake and assimilation, Li et al. generated the rice osamt1.1 null mutants using CRISPR/Cas9 technology. Compared to wild-type plants, the osamt1.1 mutants had decreased uptake capacity of potassium under low ammonium conditions, but had a higher potassium content in shoots and roots at limited potassium supply when ammonium was replete. These genetic evidences reveal that OsAMT1.1 plays an important role for maintaining the nitrogen and potassium homeostasis in rice (pp. 639e649). Recently, microRNAs (miRNAs) have been identified as the important regulatory factors in controlling nutrient starvation responses. In Arabidopsis, solexa sequencing technology has been used to detect changes in the expression patterns of miRNAs under nitrate-sufficient and nitrate-deficient conditions. The expression of four miRNAs (e.g., miR160) was significantly upregulated under nitrogen starvation conditions. Induced miR160 mediated the cleavage of ARF16 and promoted lateral root production in Arabidopsis. Interestingly, 20 novel miRNAs were identified and nine of them were responsive to nitrate starvation. To date, however, there is few genome-wide studies on rice miRNAs involved in nitrogen starvation responses. Li et al. performed high-throughput small RNA sequencing under different nitrate and ammonium conditions. The deep sequencing results clearly showed that nitrogenregulated expression patterns of miRNAs significantly differentiated between nitrate and ammonium treatments. There are 16 miRNAs induced by nitrate and 11 miRNAs induced by ammonium
http://dx.doi.org/10.1016/j.jgg.2016.11.004 1673-8527/Copyright © 2016, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and Genetics Society of China. Published by Elsevier Limited and Science Press. All rights reserved.
622
Editorial / Journal of Genetics and Genomics 43 (2016) 621e622
under short-term treatments, and there are 60 differentially expressed miRNAs between nitrate and ammonium under longterm treatments. The expression of OsmiR160 induced by ammonium was higher than that induced by nitrate, whereas miR164 was done in opposite ways. Theses comprehensive expression profiling of miRNAs in response to nitrate and/or ammonium starvation conditions presents an advance in understanding the regulation of different nitrogen signaling and homeostasis mediated by miRNAs (pp. 651e661). Unlike various nitrogen forms, phosphorus (P) forms insoluble compounds in acidic soils, or is unevenly distributed as phosphate (Pi) in alkaline soils. Thus, Pi availability in soils is often a key limiting factor for plant growth in both natural and agricultural systems. To cope with low Pi availability, plants have to reprogram gene expression profile to facilitate Pi acquisition and assimilation. Previous studies have demonstrated that AtPHR1 and OsPHR2 play the important roles in Pi signaling. Recently, crystal structures of SPX protein reveal that SPX domains function as inositol polyphosphate (InsP) sensor. InsP binding allows SPX domains to interact with transcription factors AtPHR1 and OsPHR2, and the SPX-PHR protein complex prevents AtPHR1 and OsPHR2 from binding their target promoters, which in turn regulates Pi homeostasis. In addition, plants evolve a number of developmental responses to adapt both the internal Pi status in planta and the external soil Pi availability, including changes in shoot-root ratio and formation of highly branched root systems, which enhance the exploratory capacity of roots to search for Pi-rich patches present in the soil. Thus, the improvement of root architectures is a major breeding target to enhance Pi assimilation and use efficiency. Gu et al. showed that two maize inbred lines Ye478 and Wu312 exhibited substantial variations with respect to phosphorus-use efficiency (PUE) and root system architecture (RSA). It resulted in the identification of quantitative trait loci (QTLs) presumed to determine PUE in maize. Using 218 recombination inbred lines derived from the cross between Ye478 and Wu312, Gu et al. identified two QTL-clusters Clbin3.04a and Cl-bin3.04b responsible for PUE and RSA. More importantly, combining Cl-bin3.04a and Cl-bin3.04b loci can be effective in simultaneously improving PUE and RSA in both hydroponics and field conditions. This genetic result links RSA to PUE, and provides a new strategy to improve maize PUE through QTL-based selection of root system architectures (pp. 663e672). Sulfur is also an essential plant nutrient, necessary for synthesis of many metabolites which are important for biotic and abiotic interactions of plant growth and food production in terms of both grain yield and grain quality. Inorganic sulfate (SO 4 ) is taken up from the soil by plants via their root system, which is activated by adenylation to adenosine 5'-phosphosulfate (APS) by ATP sulfurylase, and further phosphorylated to 3'-phosphoadenosine-5'phosphosulfate, which is used for sulfation reactions. Cys is the key metabolite in the synthesis of sulfur-containing compounds in plants, while the major pool of sulfur, which is not stored in proteins, is the Cys-containing peptide GSH. Koprivova and Kopriva describe recent progress in dissection of the regulatory network of sulfate uptake and homeostasis by transcriptional and posttranscriptional regulation of sulfur transport, as well as sulfur metabolism and reutilization. The perspective also describes the molecular mechanisms of how plants adapt to changes in sulfur availability, and highlights the genetic approaches to increase sulfur assimilation and use efficiency to improve crop productivity (pp. 623e629). In acidic soils, aluminum (Al) becomes more soluble and ionic Al3þ dramatically inhibits root growth and nutrients uptake, meanwhile, P fixation with Al and Fe oxides results in more severe reduction of Pi availability. Thus, plants have to evolve diverse strategies
to simultaneously cope with Al toxicity and Pi deficiency under acidic soil conditions. Chen and Liao summarize the latest advances in the understanding of the molecular mechanisms for exudation and metabolism of organic acid anions (OAs), such as malate, citrate and oxalate, which are secreted by roots into the rhizosphere to chelate Al3þ and mobilize Pi, thereby serving as a defense weapon for plants against both Al toxicity and Pi deficiency under acidic soil conditions. The exudation of OAs varies widely among various plant species and fluctuating environments, and the transporters (e.g., ALMT and MATE) responsible for OA secretion and metabolic enzymes involved in OA biosynthesis have been functionally characterized in model and crop plants. In addition, the genetic manipulation of OA metabolism and transport provides an effective way to enhance tolerance to high Al3þ and low Pi stresses, suggesting that the application of CRISPR/Cas9 genome editing technology can help to improve crop productivity in acidic soils (pp. 631e638). Unlike other macronutrients, copper (Cu) is an essential micronutrient, but it is also highly toxic to plant growth and development when in excess. Importantly, Cu has been used as a way to increase the efficiency of animal production because of the low Cu content in most sources of feed. Cu in plants is often present in complex forms bound to cysteine-rich proteins and carboxylic and phenolic groups, and its deficiency has been reported in many crops. The previous studies have shown that SBP-domain transcription factor AtSPL7 regulates Cu uptake and relocation in Arabidopsis. Tang et al. identified rice OsSPL9 with sequence homolog to AtSPL7, and generated transgenic rice plants, in which OsSPL9 was constitutively expressed. Compared to wild-type plants, the transgenic rice plants exhibited similar phenotypes with respect to root systems, plant height and grain yield. However, the up-regulation of OsSPL9 promoted the expression of several COPT genes that encode copper transporters, resulting in high-level accumulation of organic copper in grain and improvement in its digestibility, which indicates that genetic manipulation of OsSPL9 and its ortholog represents a new way toward Cu biofortification in rice (pp. 673e676). Improving plant nutrient use efficiency is essential for the development of sustainable agriculture, however, plant nutrient use efficiency is a complex trait determined by QTLs and influenced by fluctuating environments (Liu et al., 2015). These articles included in this special issue have covered several aspects of highly intergraded signaling pathways that control nutrient uptake, metabolism, and associated starvation responses. Further identification of new components that mediate nutrient signaling using genome-wide approaches and understanding of the regulatory networks and crosstalk with other phytohormone signaling pathways will help to improve nutrient use efficiency and crop productivity.
References Liu, Q., Chen, X., Wu, K., Fu, X., 2015. Nitrogen signaling and use efficiency in plants: what's new? Curr. Opin. Plant Biol. 27, 192e198. Tilman, D., Cassman, K.G., Matson, P.A., Naylor, R., Polasky, S., 2002. Agricultural sustainability and intensive production practices. Nature 418, 671e677.
Xiangdong Fu The State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China E-mail address: [email protected]. 11 November 2016 Available online 13 November 2016