REVIEW: PART OF A SPECIAL ISSUE ON PLANT NUTRITION Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeum vulgare)

† Background and Aims Research on manganese (Mn) toxicity and tolerance indicates that Mn toxicity develops apoplastically through increased peroxidase activities mediated by phenolics and Mn, and Mn tolerance could be conferred by sequestration of Mn in inert cell compartments. This comparative study focuses on Mn-sensitive barley (Hordeum vulgare) and Mn-tolerant rice (Oryza sativa) as model organisms to unravel the mechanisms of Mn toxicity and/or tolerance in monocots. † Methods Bulk leaf Mn concentrations as well as peroxidase activities and protein concentrations were analysed in apoplastic washing fluid (AWF) in both species. In rice, Mn distribution between leaf compartments and the leaf proteome using 2D isoelectic focusing IEF/SDS‐PAGE and 2D Blue native BN/SDS‐PAGE was studied. † Key Results The Mn sensitivity of barley was confirmed since the formation of brown spots on older leaves was induced by low bulk leaf and AWF Mn concentrations and exhibited strongly enhanced H2O2-producing and consuming peroxidase activities. In contrast, by a factor of 50, higher Mn concentrations did not produce Mn toxicity symptoms on older leaves in rice. Peroxidase activities, lower by a factor of about 100 in the rice leaf AWF compared with barley, support the view of a central role for these peroxidases in the apoplastic expression of Mn toxicity. The high Mn tolerance of old rice leaves could be related to a high Mn binding capacity of the cell walls. Proteomic studies suggest that the lower Mn tolerance of young rice leaves could be related to Mn excess-induced displacement of Mg and Fe from essential metabolic functions. † Conclusions The results provide evidence that Mn toxicity in barley involves apoplastic lesions mediated by peroxidases. The high Mn tolerance of old leaves of rice involves a high Mn binding capacity of the cell walls, whereas Mn toxicity in less Mn-tolerant young leaves is related to Mn-induced Mg and Fe deficiencies.

[1]  Changming Dou,et al.  Accumulation and detoxification of manganese in hyperaccumulator Phytolacca americana. , 2009, Plant biology.

[2]  A. van Dorsselaer,et al.  Characterization of leaf apoplastic peroxidases and metabolites in Vigna unguiculata in response to toxic manganese supply and silicon , 2009, Journal of experimental botany.

[3]  Xiyan Li,et al.  A Distinct Endosomal Ca2+/Mn2+ Pump Affects Root Growth through the Secretory Process1[C][W][OA] , 2008, Plant Physiology.

[4]  N. Yamaji,et al.  Functions and transport of silicon in plants , 2008, Cellular and Molecular Life Sciences.

[5]  A. van Dorsselaer,et al.  Early manganese‐toxicity response in Vigna unguiculata L. – a proteomic and transcriptomic study , 2008, Proteomics.

[6]  W. Horst,et al.  LEAF SENESCENCE AND N UPTAKE PARAMETERS AS SELECTION TRAITS FOR NITROGEN EFFICIENCY OF OILSEED RAPE CULTIVARS , 2007 .

[7]  Matias D. Zurbriggen,et al.  Enhanced plant tolerance to iron starvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin , 2007, Proceedings of the National Academy of Sciences.

[8]  J. Pittman,et al.  A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. , 2007, The Plant journal : for cell and molecular biology.

[9]  S. Husted,et al.  A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance , 2007, Proceedings of the National Academy of Sciences.

[10]  H. Braun,et al.  The Role of the Leaf Apoplast in Manganese Toxicity and Tolerance in Cowpea ( Vigna Unguiculata L. Walp) , 2007 .

[11]  Naoki Yamaji,et al.  Silicon uptake and accumulation in higher plants. , 2006, Trends in plant science.

[12]  I. E. Woodrow,et al.  In vivo localization of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. , 2006, Plant, cell & environment.

[13]  M. Yano,et al.  A silicon transporter in rice , 2006, Nature.

[14]  J. Pittman Managing the manganese: molecular mechanisms of manganese transport and homeostasis. , 2005, The New phytologist.

[15]  D. Williams,et al.  Iron and manganese relations in rice and barley , 1964, Plant and Soil.

[16]  U. Feller,et al.  Biochemical changes in barley plants after excessive supply of copper and manganese , 2004 .

[17]  M. G. Barreiro,et al.  Manganese accumulation in rice: implications for photosynthetic functioning. , 2004, Journal of plant physiology.

[18]  E. Delhaize,et al.  Engineering high-level aluminum tolerance in barley with the ALMT1 gene. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Lothar Jänsch,et al.  Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. , 2004, Phytochemistry.

[20]  M. Fujita,et al.  Proteomics of the rice cell: systematic identification of the protein populations in subcellular compartments , 2004, Molecular Genetics and Genomics.

[21]  T. Mansfeldt Redox potential of bulk soil and soil solution concentration of nitrate, manganese, iron, and sulfate in two Gleysols , 2004 .

[22]  Fusuo Zhang,et al.  Effect of iron plaque outside roots on nutrient uptake by rice (Oryza sativa L.). Zinc uptake by Fe-deficient rice , 1998, Plant and Soil.

[23]  W. Horst,et al.  Effect of light intensity on manganese toxicity symptoms and callose formation in cowpea (Vigna unguiculata (L.) Walp.) , 1992, Plant and Soil.

[24]  W. Horst,et al.  Effects of silicon supply on apoplastic manganese concentrations in leaves and their relation to manganese tolerance in cowpea (Vigna unguiculata (L.) Walp.) , 2004, Plant and Soil.

[25]  P. Wu,et al.  Molecular marker analysis of manganese toxicity tolerance in rice under greenhouse conditions , 2004, Plant and Soil.

[26]  H. Braun,et al.  Effect of Manganese Toxicity on the Proteome of the Leaf Apoplast in Cowpea1 , 2003, Plant Physiology.

[27]  G. Kirk Rice root properties for internal aeration and efficient nutrient acquisition in submerged soil. , 2003, The New phytologist.

[28]  E. Delhaize,et al.  Genes Encoding Proteins of the Cation Diffusion Facilitator Family That Confer Manganese Tolerance Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009134. , 2003, The Plant Cell Online.

[29]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[30]  W. Horst,et al.  APOPLASTIC PEROXIDASES AND ASCORBATE ARE INVOLVED IN MANGANESE TOXICITY AND TOLERANCE OF VIGNA UNGUICULATA , 2003 .

[31]  W. Frommer,et al.  A Putative Role for the Vacuolar Calcium/Manganese Proton Antiporter AtCAX2 in Heavy Metal Detoxification , 2002 .

[32]  M. Sussman,et al.  An Endoplasmic Reticulum-Bound Ca2+/Mn2+Pump, ECA1, Supports Plant Growth and Confers Tolerance to Mn2+ Stress1 , 2002, Plant Physiology.

[33]  V. Römheld,et al.  Role of leaf apoplast in silicon‐mediated manganese tolerance of Cucumis sativus L. , 2002 .

[34]  K. Iwasaki,et al.  Leaf apoplastic silicon enhances manganese tolerance of cowpea (Vigna unguiculata) , 2002 .

[35]  M. Hajduch,et al.  High‐resolution two‐dimensional electrophoresis separation of proteins from metal‐stressed rice (Oryza sativa L.) leaves: Drastic reductions/ fragmentation of ribulose‐1,5‐bisphosphate carboxylase/oxygenase and induction of stress‐related proteins , 2001, Electrophoresis.

[36]  F. Lidon Tolerance of rice to excess manganese in the early stages of vegetative growth. Characterisation of manganese accumulation , 2001 .

[37]  F. Lidon,et al.  Rice tolerance to excess Mn: Implications in the chloroplast lamellae and synthesis of a novel Mn protein , 2000 .

[38]  K. Hirschi,et al.  Expression of arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. , 2000, Plant physiology.

[39]  W. Horst,et al.  Physiology of manganese toxicity and tolerance in Vigna unguiculata (L.) Walp. , 1999 .

[40]  P. Weisbeek,et al.  Iron‐dependent stability of the ferredoxin I transcripts from the cyanobacterial strains Synechococcus species PCC 7942 and Anabaena species PCC 7937 , 1993, Molecular microbiology.

[41]  V. Neuhoff,et al.  Essential problems in quantification of proteins following colloidal staining with Coomassie Brilliant Blue dyes in polyacrylamide gels, and their solution , 1990, Electrophoresis.

[42]  E. Schlichting,et al.  Distribution and Amelioration of Manganese Toxic Soils , 1988 .

[43]  J. Burnell The Biochemistry of Manganese in Plants , 1988 .

[44]  R. Dernick,et al.  Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels , 1988, Electrophoresis.

[45]  H. Marschner Mineral Nutrition of Higher Plants , 1988 .

[46]  W. Hurkman,et al.  Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. , 1986, Plant physiology.

[47]  V. Neuhoff,et al.  Clear background and highly sensitive protein staining with Coomassie Blue dyes in polyacrylamide gels: A systematic analysis , 1985 .

[48]  C. Foy Physiological Effects of Hydrogen, Aluminum, and Manganese Toxicities in Acid Soil , 2015 .

[49]  L. E. Nelson Tolerances of 20 Rice Cultivars to Excess Al and Mn1 , 1983 .

[50]  W. Horst Quick screening of cowpea genotypes for manganese tolerance during vegetative and reproductive growth , 1982 .

[51]  R. Miller,et al.  Adenosine kinase from rabbit liver. I. Purification by affinity chromatography and properties. , 1979, The Journal of biological chemistry.

[52]  R. Chaney,et al.  The Physiology of Metal Toxicity in Plants , 1978 .

[53]  J. Anderson Adenylate metabolism of embryonic axes from deteriorated soybean seeds. , 1977, Plant physiology.

[54]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[55]  D. Heenan,et al.  Tolerance of Soybean Cultivars to Manganese Toxicity1 , 1976 .

[56]  A. Felsani,et al.  Formation of active hybrid 80-S particles from subunits of pea seedlings and mammalian liver ribosomes. , 1972, Biochimica et biophysica acta.

[57]  D. Williams,et al.  Ion Competition in Manganese Uptake by Barley Plants. , 1962, Plant physiology.