Mutational loss of Arabidopsis SLOW WALKER2 results in reduced endogenous spermine concomitant with increased aluminum sensitivity
Cynthia D. Nezames A , Vanessa Ochoa A and Paul B. Larsen A B
+ Author Affiliations
- Author Affiliations
A Department of Biochemistry, University of California-Riverside, Riverside, CA 92521, USA.
B Corresponding author. Email: paul.larsen@ucr.edu
Functional Plant Biology 40(1) 67-78 https://doi.org/10.1071/FP12234
Submitted: 4 August 2012 Accepted: 20 September 2012 Published: 2 November 2012
Abstract
A previously-identified Arabidopsis mutant with hypersensitivity to aluminum, als7–1 was studied further to determine the nature of the mutation and subsequently establish the biochemical basis of the increase in Al sensitivity. Physiological analysis revealed that the Al hypersensitivity phenotype is correlated with increased Al uptake and Al-dependent gene expression, indicating that als7–1 has a defect in an Al-exclusion mechanism. Cloning of the als7–1 mutation showed that it negatively affects the gene encoding the putative nucleolar localised ribosomal biogenesis factor SLOW WALKER2, which is required for normal gametogenesis and mitotic progression. Molecular analysis indicated that Al hypersensitivity in als7–1 is correlated with loss of expression of a factor required for S-adenosylmethionine recycling and reduced levels of endogenous polyamines in the mutant. Further analysis shows that Al-dependent root growth inhibition is reversed by addition of exogenous spermine, which is correlated with a significant reduction in Al uptake by spermine treated roots. Endogenous spermine likely functions to compete with Al3+ for binding to extra- and intracellular anionic sites, which suggests that increased spermine levels may be an effective means to improve root growth in Al toxic acid soil environments.
Additional keywords: als7, aluminum, aluminium, polyamines, spermine, swa2.
References
Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Salinas J, Tiburcio AF, Altabella T (2011) Integration of polyamine in the cold acclimation response. Plant Science 180, 31–38.| Integration of polyamine in the cold acclimation response.Crossref | GoogleScholarGoogle Scholar |
Bürstenbinder K, Rzewuski G, Wirtz M, Hell R, Sauter M (2007) The role of methionine recycling for ethylene synthesis in Arabidopsis. The Plant Journal 49, 238–249.
| The role of methionine recycling for ethylene synthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Chen W, Xu C, Zhao B, Wang X, Wang Y (2008) Improved Al tolerance of saffron (Crocus sativus L.) by exogenous polyamines. Acta Physiologiae Plantarum 30, 121–127.
| Improved Al tolerance of saffron (Crocus sativus L.) by exogenous polyamines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVaktLg%3D&md5=897c5e898b9a29ee18ad03bb94a1b970CAS |
Degenhardt J, Larsen PB, Howell SH, Kochian LV (1998) Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiology 117, 19–27.
| Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsFSksL0%3D&md5=fd41c243c7c4df7584708f316834a876CAS |
Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology 103, 695–702.
Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant & Cell Physiology 48, 1081–1091.
| An aluminum-activated citrate transporter in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKlsrrK&md5=f14ba216bdaa7539c7b40cdb9f4b5767CAS |
Gilbert RS, Gonzalez GG, Hawel L, Byus CV (1991) An ion-exchange chromatography procedure for the isolation and concentration of basic amino acids and polyamines from complex biological samples prior to high-performance liquid chromatography. Analytical Biochemistry 199, 86–92.
| An ion-exchange chromatography procedure for the isolation and concentration of basic amino acids and polyamines from complex biological samples prior to high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslCqsrc%3D&md5=0e43f69531dede485638a46d0c3c439aCAS |
Henikoff S, Till BJ, Comai L (2004) TILLING. Traditional mutagenesis meets functional genomics. Plant Physiology 135, 630–636.
| TILLING. Traditional mutagenesis meets functional genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlKjtb0%3D&md5=b66db6fb0e6443fb141a915168a41b26CAS |
Hoekenga OA, Maron LG, Pineros MA, Cancado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 9738–9743.
| AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVOntrY%3D&md5=59f2eb3ae8938c0c1f1018504b0bfb9bCAS |
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant & Cell Physiology 45, 712–722.
| Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlWrtbg%3D&md5=e4586a46dc8b89789a07deaa0373b162CAS |
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 46, 237–260.
| Cellular mechanisms of aluminum toxicity and resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsVCqtb0%3D&md5=e7e4ee56bbf78cfb77146e2b46190a07CAS |
Larsen PB, Tai CY, Kochian LV, Howell SH (1996) Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiology 110, 743–751.
| Arabidopsis mutants with increased sensitivity to aluminum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhs1Gis7s%3D&md5=05b6a9b6b06b7296828aad108297bdceCAS |
Larsen PB, Geisler MJB, Jones CA, Williams KM, Cancel JD (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. The Plant Journal 41, 353–363.
| ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVKns7w%3D&md5=24a454bbb198654586667a6eb912a45eCAS |
Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225, 1447–1458.
| Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlOhtLY%3D&md5=cfb1a6b55df60412378fa5a946cd28feCAS |
Li N, Yuan L, Liu N, Shi D, Li X, Tang Z, Liu J, Sundaresan V, Yang WC (2009) SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progression during female gametophyte development in Arabidopsis. Plant Physiology 151, 1486–1497.
| SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progression during female gametophyte development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjsbbM&md5=afb22826d279273fea95b5e552384728CAS |
Lum LSY, Sultzman LA, Kaufman RJ, Linzer DIH, Wu BJ (1990) A cloned human CCAAT-box-binding factor stimulates transcription from the human hsp70 promoter. Molecular and Cellular Biology 10, 6709–6717.
Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39, 1156–1161.
| A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXps12gtL8%3D&md5=8e50e9f4395d25b7a60163e850a2beb9CAS |
Minocha R, Minocha SC, Long SL, Shortle WC (1992) Effects of aluminum on DNA synthesis, cellular polyamines, polyamine biosynthetic enzymes and inorganic ions in cell suspension cultures of a woody plant Catharanthus roseus. Physiologia Plantarum 85, 417–424.
| Effects of aluminum on DNA synthesis, cellular polyamines, polyamine biosynthetic enzymes and inorganic ions in cell suspension cultures of a woody plant Catharanthus roseus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Oi&md5=e9fe72a181a4a0a0eca58991575f28bdCAS |
Nezames CD, Sjogren CA, Barajas JF, Larsen PB (2012) The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. The Plant Cell 24, 608–621.
| The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xns1elsrc%3D&md5=70c5905280412ddfa5a2800e76994b85CAS |
Rounds MA, Larsen PB (2008) Aluminum dependent root growth inhibition results from AtATR dependent cell cycle arrest and loss of the quiescent center in Arabidopsis. Current Biology 18, 1495–1500.
| Aluminum dependent root growth inhibition results from AtATR dependent cell cycle arrest and loss of the quiescent center in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1entL7M&md5=f56ba7257a56bf6e5f10cd2e18f94c91CAS |
Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal 37, 645–653.
| A wheat gene encoding an aluminum-activated malate transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXislyltr4%3D&md5=bac4bc782bee24ae0d1e0a09d74e37d9CAS |
Takahashi T, Kakehi J (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Annals of Botany 105, 1–6.
| Polyamines: ubiquitous polycations with unique roles in growth and stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFyksb7K&md5=605c1922e69f20e490e9579363b770c5CAS |
Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochemical and Biophysical Research Communications 313, 369–375.
| Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVWmtb4%3D&md5=d2013d22d50593fe1cde5449d1d1358dCAS |
Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Letters 579, 1557–1564.
| Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslCisL8%3D&md5=df845cd0a2d8567dc4abac0571bae9e6CAS |
von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant and Soil 171, 1–15.
| Global extent, development and economic impact of acid soils.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochemical and Biophysical Research Communications 352, 486–490.
| A protective role for the polyamine spermine against drought stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlShsr3O&md5=2f6276f5a03c44ef1f914dbf47b12f0fCAS |
Zdobnov EM, Apweiler R (2001) InterProScan – an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847–848.
| InterProScan – an integration platform for the signature-recognition methods in InterPro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFehsro%3D&md5=7ec77af1b24565cab98b5de70b1021f4CAS |
