Mineral nutrients taken up from the soil become incorporated into a variety of important compounds with structural and physiological roles in plants. We summarize how plant nutrients are linked to many metabolic pathways, plant hormones and other biological processes. We also focus on nutrient uptake, describing plant���microbe interactions, plant exudates, root architecture, transporters and their applications. Plants need to survive in soils with mineral concentrations that vary widely. Describing the relationships between nutrients and biological processes will enable us to understand the molecular basis for signaling, physiological damage and responses to mineral stresses. Keywords: Cross-talk ��� Microorganisms ��� Omics ��� Plant nutrition ��� Soil ��� Transporter . Abbreviations : ALMT , aluminum-activated malate transporter AMF , arbuscular mycorrhizal fungi CS , citrate synthase ICDH , isocitrate dehydrogenase JA , jasmonate MA , mugineic acid MATE , multidrug and toxic compound extrusion NAAT , nicotianamine aminotransferase OAS , O -acetyl- L -serine PEPC , phosphoenolpyruvate carboxylase PGPR , plant growth- promoting rhizobacteria. Cross-Talk Between Plant Nutrients and Their Relationship to Other Physiological Processes Plants produce organic matter from mineral elements absorbed from the soil and atmosphere. Thus, the essential elements are fundamentally important for plant physiology. Plants require 17 essential elements for completion of their life cycle, namely C, H, O, Ca, K, Mg, N, S, P, Cl, B, Cu, Fe, Mn, Mo, Ni and Zn. Deprivation of even one of these essential elements causes physiological disorders, e.g. cell death under B depriva- tion ( Koshiba et al. 2009 ). Elements that stimulate growth and may be essential to particular species are defi ned as benefi cial elements. The fi ve most investigated benefi cial elements are Al, Co, Na, Se and Si ( Pilon-Smits et al. 2009 ). The availability of plant genome sequences and the development of molecular biological techniques have accelerated the identifi cation of pathways assimilating these elements and the genes responsi- ble, and now focus is moving towards the regulation of these pathways and cross-talk between them. The fi rst part of this review describes the cross-talk between nutritional metabolic pathways and how they are linked to other metabolic pathways and biological processes, exemplifying recent ���omics��� analyses and other studies relating to S, N and P. Sulfur (S) A link between S and N metabolism has been known for many years, with deprivation of one disrupting the metabolism of the other ( Reuveny et al. 1980 , Prosser et al. 2001 ). Using the sulfur-responsive seed storage protein gene as a model, Kim et al. (1999) showed that O -acetyl- L -serine (OAS), the direct precursor of cysteine synthesis in higher plants, is a key media- tor of sulfur and nitrogen nutrition-regulated gene expression. OAS is located at the convergence of the S and N assimilation pathways, and its concentration changes in response to the N/S ratio in the growth medium. Hirai et al. (2003 , 2004) showed a good correlation in the transcript and metabolite profi les produced by S defi ciency ( ��� S) with those produced by OAS treatment. The role of OAS as a regulator of S-responsive genes was also demonstrated by an Arabidopsis mutant accu- mulating OAS ( Ohkama-Ohtsu et al. 2004 ). Transcriptomic and metabolomic analyses in response to ��� S uncovered a connection between S nutrition and other metabolic pathways ( Hirai et al. 2003 , Maruyama-Nakashita et al. 2003 , Nikiforova et al. 2003 , Hirai et al. 2004 , Nikiforova et al. 2005 ). The early response to ��� S caused a decrease in cysteine and glutathione (GSH), and accumulation of their precursors OAS and serine. The increase in serine was chan- neled to tryptophan. Accumulation of tryptophan led in turn to an increase in auxin, probably via indole glucosinolate catabolism, which might trigger root elongation to elevate accessibility to exogenous S. Biosynthesis of another plant hormone, jasmonate (JA), was also induced by ��� S. Interestingly JA treatment enhanced S assimilation ( Sasaki-Sekimoto et al. 2005 ), implying the involvement of JA in the ��� S response. While these early responses are considered to be for adaptation, Recent Progress in Plant Nutrition Research: Cross-Talk Between Nutrients, Plant Physiology and Soil Microorganisms Naoko Ohkama-Ohtsu 1 and Jun Wasaki 2 , * 1 United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Saiwai-cho 3-5-8, Fuchu, Tokyo, 183-8509 Japan 2 Graduate School of Biosphere Science, Hiroshima University, Kagamiyama 1-7-1, Higashi-Hiroshima, 739-8521 Japan * Corresponding author: E-mail, junw@hiroshima-u.ac.jp Fax, + 81-82-424-4370 (Received March 15, 2010 Accepted July 2, 2010) Plant Cell Physiol. 51(8): 1255���1264 (2010) doi:10.1093/pcp/pcq095, available online at www.pcp.oxfordjournals.org �� The Author 2010. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org 1255 Plant Cell Physiol. 51(8): 1255���1264 (2010) doi:10.1093/pcp/pcq095 �� The Author 2010. Mini Review at Universitaetsbibliothek Giessen on July 18, 2011 pcp.oxfordjournals.org Downloaded from

long-term ��� S caused physiological disorders resulting from the stress. Long-term ��� S decreased levels of chlorophyll this may be caused by decrease in an S-containing metabolite, because S -adenosyl-methionine is required in a late step of chlorophyll biosynthesis. An overall decline in lipid content was likely to be caused by a block in fatty acid synthesis. Two S-containing molecules, acetyl-CoA and acyl carrier protein, are involved in fatty acid synthesis, thus lipid breakdown may be explained by limitation of these S-containing molecules. Long-term ��� S also induced the catabolism of purine and pyrimidine bases and biosynthesis of ureides, presumably to store excess N and detoxify ammonium. GSH, a tripeptide of �� -Glu���Cys���Gly, is a good example to illustrate how S nutrition is linked to various biological processes. GSH is thought to be a signal molecule, transmitting S status through the phloem to regulate S assimilation ( Lappartient et al. 1999 ). In addition it is a major storage and transport form of organic S, as cysteine produced by GSH degradation is used for the synthesis of proteins and other S-containing metabolites ( Leustek 2000 ). A recent study dem- onstrated that GSH is also a source of glutamate ( Ohkama-Ohtsu et al. 2008 , Ohkama-Ohtsu et al. 2009 ). Besides its role in S and N metabolism, GSH plays important roles in cellular redox homeostasis. As a component of the ascorbate���GSH cycle, or though the action of GSH peroxidase, GSH detoxifi es H 2 O 2 ( Noctor and Foyer 1998 , Foyer and Noctor 2005 , Foyer and Noctor 2009 ). The ascorbate���GSH cycle also functions in the defense against heavy metals ( Paradiso et al. 2008 ). An Arabi- dopsis mutant with elevated levels of oxidized glutathione (GSSG) in the apoplast revealed that the redox balance main- tained by GSH in the apoplast is important to alleviate oxidative stress ( Ohkama-Ohtsu et al. 2007 , Ohkama-Ohtsu et al. 2009 ). Furthermore, GSH is involved in the regulation of enzymes by reacting with cysteine residues in proteins and thereby altering their folding. The reversible glutathionylation of cysteine residues in proteins, modulated by glutaredoxins, can control enzyme activity and also acts as part of the signal transduction mechanism as plants respond to oxidative stress ( Rouhier et al. 2008 , Foyer and Noctor 2009 ). Redox status regulated by GSH is also likely to be an important factor in plant cell cycle regulation. Arabidopsis plants homozygous for a mutation in the ROOT MERISTEMLESS1 ( RML1 ) gene were unable to establish an active post-embryonic meristem in the root apex ( Vernoux et al. 2000 ). The RML1 gene encodes the fi rst enzyme of GSH biosynthesis, �� -glutamylcysteine syn- thetase, and rml1 mutants contained only 3 % of the extract- able GSH compared with those of the wild type. Vernoux et al. (2000) showed that the G 1 to S phase transition requires an adequate level of GSH, and depletion of GSH caused down- regulation of cell cycle genes. In animal cells, mitogenic signal- ing pathways activated by growth factors which converge on core cell cycle regulators have been shown to be redox depen- dent ( Burhans and Heintz 2009 ), and such transduction path- ways mediated by GSH may also exist in plant cells. rml1 mutants with residual amounts of GSH are able to germinate. However, in T-DNA insertion mutants in the �� -glutamylcysteine synthetase gene, GSH is completely absent and the mutants are embryo lethal. Analysis of these null mutants demonstrated that GSH biosynthesis within the embryo is required for proper seed maturation ( Cairns et al. 2006 ). Studies with another allelic mutant, pad2-1 , which contains about 20 % of the GSH found in wild-type plants, suggested the involvement of GSH in defense against pathogens and insects. pad2-1 accumulated lower amounts of camalexin, a phytoalexin of Arabidopsis, and glucosinolates, a defense compound against herbivores, although it is not completely clear how GSH regulates the amounts of these compounds ( Parisy et al. 2007 , Schlaeppi et al. 2008 ). GSH also appears to be a determinant of fl owering, and its synthesis is induced by vernalization ( Ogawa et al. 2001 , Ogawa et al. 2004 , Yanagida et al. 2004 ). Change in the redox state of GSH regulates the differentiation of tracheary elements ( Henmi et al. 2005 ). Nitrogen (N) Transcriptome analyses of the plant response to nitrate revealed links not only between N and S, but also between N and Fe ( Wang et al. 2003 ). Application of nitrate in N-starved plants induced nicotianamine synthase genes, which are involved in Fe acquisition, transport and homeostasis in plants ( von Wiren et al. 1999 , Pich et al. 2001 ). Fe is required for the activity of many of the enzymes in nitrate assimilation, including nitrate reductase, nitrite reductase and ferredoxin. Therefore, the nitrate-induced nicotianamine synthesis probably occurs in order to facilitate Fe transport to support the synthesis of proteins for nitrate assimilation. Scheible et al. (2004) extended the analysis by combining transcript levels with metabolite concentrations. They analyzed both the rapid response (30 min) and slower response (3 h after nitrate readdition to N-starved seedlings). Nitrate was increased in seedlings within 10 min, but glutamate, glutamine, starch, sugars, 2-oxoglutarate and medium pH were unchanged after 30 min. At 30 min after nitrate readdition, genes for nitrate uptake and assimilation were strongly induced, coinciding with the induction of genes needed to provide reducing equivalents, such as genes for production of NADH or reduced ferredoxin. Genes required for the production of organic acids, which act as acceptors of assimilated nitrate and as counter anions to replace nitrate and maintain the pH balance ( Scheible et al. 1997 ), were rapidly induced. These changes were followed by induction of genes promoting the synthesis of amino acids, purines and pyrimidines, and conversely the repression of genes promoting breakdown of these compounds. Slower responses included the induction of genes involved further downstream in N use, such as the synthesis of RNAs, proteins and cell walls. As for lipid metabolism, genes for galactolipid synthesis were repressed by nitrate readdition, meaning that plants save the N contained in the polar group under N starvation, just as they save the P contained in the polar group under P starvation. Nitrate readdition led to coordinated repression of the genes for phenylpropanoid and fl avonoid metabolism. This was 1256 N. Ohkama-Ohtsu and J. Wasaki Plant Cell Physiol. 51(8): 1255���1264 (2010) doi:10.1093/pcp/pcq095 �� The Author 2010. at Universitaetsbibliothek Giessen on July 18, 2011 pcp.oxfordjournals.org Downloaded from