Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 17, 2017, Pages E3563-E3572

  Mora Macías, Javier ^a   Ojeda Rivera, Jonathan Odilón ^a   Gutiérrez Alanís, Dolores ^a   Yong Villalobos, Lenin ^a   Oropeza Aburto, Araceli ^a   Raya González, Javier ^a   Jiménez Domínguez, Gabriel ^a   Chávez Calvillo, Gabriela ^a   Rellán Álvarez, Rubén ^a   Herrera Estrell, Luis ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

Cell differentiation; Gene regulation; Iron; Phosphate; Root response

Indexed keywords

ALUMINUM ACTIVATED MALATE TRANSPORTER 1; IRON; MALIC ACID; MEMBRANE PROTEIN; PHOSPHATE; PLANT DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR STOP1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ALMT1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; MALIC ACID DERIVATIVE; ORGANIC ANION TRANSPORTER; STOP1 PROTEIN, ARABIDOPSIS;

ABIOTIC STRESS; ALLELE; AMINO ACID SUBSTITUTION; APOPLAST; ARABIDOPSIS THALIANA; ARTICLE; CELL DIFFERENTIATION; ENVIRONMENTAL STRESS; GENE CONTROL; GENE MAPPING; GENE MUTATION; GENETIC CODE; LPI5 GENE; LPI6 GENE; MUTANT; NONHUMAN; PHENOTYPE; PLANT CELL; PLANT DEVELOPMENT; PLANT GENOME; PRIORITY JOURNAL; ROOT GROWTH; ROOT SYSTEM; TRANSCRIPTOMICS; ARABIDOPSIS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; IRON; MALATES; MERISTEM; ORGANIC ANION TRANSPORTERS; PHOSPHATES; TRANSCRIPTION FACTORS;

EID: 85018845915     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1701952114     Document Type: Article

References (51)

1. Marschner H (2011) Marschner's Mineral Nutrition of Higher Plants (Elsevier Science, Amsterdam, The Netherlands).
2. Wu P, et al. (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260-1271.
3. Misson J, et al. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934-11939.
4. Morcuende R, et al. (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85-112.
5. Thibaud MC, et al. (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775-789.
6. Bustos R, et al. (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:e1001102.
7. Hoffland E, Van Den Boogaard R, Nelemans J, Findenegg G (1992) Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol 122:675-680.
8. Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103:6765-6770.
9. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529-538.
10. López-Bucio J, et al. (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244-256.
11. Sánchez-Calderón L, et al. (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174-184.
12. Péret B, Clément M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16:442-450.
13. Rubio V, et al. (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15: 2122-2133.
14. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665-693.
15. Sánchez-Calderón L, et al. (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 140:879-889.
16. Svistoonoff S, et al. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792-796.
17. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147:1181-1191.
18. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801-814.
19. Ticconi CA, et al. (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci USA 106:14174-14179.
20. Müller J, et al. (2015) Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell 33:216-230.
21. Iuchi S, et al. (2007) Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA 104:9900-9905.
22. Hoekenga OA, et al. (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738-9743.
23. Kobayashi Y, et al. (2007) Characterization of AtALMT1 expression in aluminuminducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol 145:843-852.
24. Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503-508.
25. Sabatini S, et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463-472.
26. Sawaki Y, et al. (2009) STOP1 regulates multiple genes that protect arabidopsis from proton and aluminum toxicities. Plant Physiol 150:281-294.
27. TokizawaM, et al. (2015) SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and other transcription factors are involved in ALUMINUMACTIVATED MALATE TRANSPORTER1 expression. Plant Physiol 167:991-1003.
28. Jones DL (1998) Organic acids in the rhizosphere: A critical review. Plant Soil 205:25-44.
29. Grillet L, et al. (2014) Ascorbate efflux as a new strategy for iron reduction and transport in plants. J Biol Chem 289:2515-2525.
30. Rellán-Alvarez R, et al. (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: New insights into plant iron long-distance transport. Plant Cell Physiol 51:91-102.
31. Ziegler J, et al. (2016) Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J Exp Bot 67:1421-1432.
32. Puga MI, et al. (2014) SPX1 is a phosphate-dependent inhibitor of Phosphate Starvation Response 1 in Arabidopsis. Proc Natl Acad Sci USA 111:14947-14952.
33. Hoehenwarter W, et al. (2016) Comparative expression profiling reveals a role of the root apoplast in local phosphate response. BMC Plant Biol 16:106.
34. Francoz E, et al. (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15-21.
35. Tanz SK, et al. (2013) SUBA3: A database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 41:D1185-D1191.
36. Chacón-López A, Ibarra-Laclette E, Sánchez-Calderón L, Gutiérrez-Alanis D, Herrera-Estrella L (2011) Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation. Plant Signal Behav 6:382-392.
37. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606-616.
38. Li W, Lan P (2015) Genome-wide analysis of overlapping genes regulated by iron deficiency and phosphate starvation reveals new interactions in Arabidopsis roots. BMC Res Notes 8:555.
39. Torabinejad J, Donahue JL, Gunesekera BN, Allen-Daniels MJ, Gillaspy GE (2009) VTC4 is a bifunctional enzyme that affects myoinositol and ascorbate biosynthesis in plants. Plant Physiol 150:951-961.
40. Thieme CJ, et al. (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat Plants 1:15025.
41. Kosman DJ (2010) Redox cycling in iron uptake, efflux, and trafficking. J Biol Chem 285:26729-26735.
42. Luna E, et al. (2011) Callose deposition: A multifaceted plant defense response. Mol Plant Microbe Interact 24:183-193.
43. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329: 1065-1067.
44. Abe A, et al. (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174-178.
45. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120.
46. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
47. Li H, et al.; 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
48. Danecek P, et al.; 1000 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27:2156-2158.
49. Cingolani P, et al. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6:80-92.
50. Robinson JT, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29:24-26.
51. Yong-Villalobos L, et al. (2015) Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc Natl Acad Sci USA 112:E7293-E7302.