Title: Sensing, signaLling, and CONTROL of phosphate starvation in plants: molecular players and applications
Abstract: Chapter 2 Sensing, signaLling, and CONTROL of phosphate starvation in plants: molecular players and applications Wolf-Rüdiger Scheible, Wolf-Rüdiger Scheible Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USASearch for more papers by this authorMonica Rojas-Triana, Monica Rojas-Triana Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USASearch for more papers by this author Wolf-Rüdiger Scheible, Wolf-Rüdiger Scheible Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USASearch for more papers by this authorMonica Rojas-Triana, Monica Rojas-Triana Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, Oklahoma, USASearch for more papers by this author Book Editor(s):William C. Plaxton, William C. Plaxton Department of Biology, Queen's University, Kingston, Ontario, CanadaSearch for more papers by this authorHans Lambers, Hans Lambers School of Plant Biology, University of Western Australia, Crawley (Perth), AustraliaSearch for more papers by this author First published: 14 April 2015 https://doi.org/10.1002/9781118958841.ch2Citations: 9 AboutPDFPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShareShare a linkShare onEmailFacebookTwitterLinkedInRedditWechat Summary The availability of phosphorus (P) often limits plant growth and deve-lopment. Whilst large amounts of P-fertilizers are thus used in agricultural production systems, they are a considerable cost factor, and the runoff of excessive P causes environmental damage. Moreover, global P-reserves may last for only several more generations. Cutting down on the use of P-fertilizers therefore is important, and to ultimately do so it is crucial to understand how plants sense, signal, respond to and cope with P-limitation, to determine the genes and molecular mechanisms involved, and to apply the knowledge to improve P-acquisition and P-use efficiency (PAE, PUE) of crop plant species. This chapter provides an overview of the players involved in plant P-status signalling/sensing, and outlines the approaches used to increase PAE/PUE on the basis of understanding the plant P-starvation response and the underlying signalling pathways and networks. References Abel, S., Ticconi, C.A., & Delatorre, C.A. (2002). Phosphate sensing in vascular plants. Physiologia Plantarum 115, 1–8. Acevedo-Hernández, G., Oropeza-Aburto, A., & Herrera-Estrella, L. (2012). A specific variant of the PHR1 binding site is highly enriched in the Arabidopsis phosphate-responsive phospholipase DZ2 coexpression network. Plant Signaling & Behavior 7, 914–917. Akiyama, K., Matsuzaki, K.-i., & Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827. Al-Ghazi, Y., Muller, B., Pinloche, S., et al. (2003). Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant, Cell & Environment 26, 1053–1066. Allen, E., Xie, Z., Gustafson, A.M., & Carrington, J.C. (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221. Andersson, H., Bergström, L., Djodjic, F. et al. (2013). Topsoil and subsoil properties influence phosphorus leaching from four agricultural soils. Journal of Environmental Quality 42, 455–463. Araya, T., Miyamoto, M., Wibowo, J., et al. (2014). CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 111, 2029–2034. Atkins, C., Smith, P.C., & Rodriguez-Medina, C. (2011). Macromolecules in phloem exudates – a review. Protoplasma 248, 165–172. Aung, K., Lin, S.-I., Wu, C.-C., et al. (2006). pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology 141, 1000–1011. Baek, D., Kim, M.C., Chun, H.J., et al. (2013). Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis . Plant Physiology 161, 362–373. Balzergue, C., Puech-Pagès, V., Bécard, G., et al. (2011). The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. Journal of Experimental Botany 62, 1049–1060. Bari, R., Datt Pant, B., Stitt, M., et al. (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988–999. Bariola, P.A., Howard, C.J., Taylor, C.B., et al. (1994). The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant Journal 6, 673–685. Bates, R. & Lynch, J.P. (2001). Root hairs confer a competitive advantage under low phosphate availability. Plant and Soil 236, 243–250. Bates, T.R. & Lynch, J.P. (1996). Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19, 529–538. Bayle, V., Arrighi, J.F., Creff, A., et al. (2011). Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23, 1523–1535. Berkowitz, O., Jost, R., Kollehn, D.O., et al. (2013). Acclimation responses of Arabidopsis thaliana to sustained phosphite treatments. Journal of Experimental Botany 64, 1731–1743. Besserer, A., Puech-Pagès, V., Kiefer, P., et al. (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology 4, 1239–1247. Borch, K., Bouma, T.J., Lynch, J.P., et al. (1999). Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant, Cell & Environment 22, 425–431. Boursiac, Y., Léran, S., Corratgé-Faillie, C., et al. (2013). ABA transport and transporters. Trends in Plant Science 18, 325–333. Branscheid, A., Sieh, D., Pant, B.D., et al. (2010). Expression pattern suggests a role of miR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Molecular Plant-Microbe Interactions 23, 915–926. Breuillin, F., Schramm, J., Hajirezaei, M., et al. (2010). Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant Journal 64, 1002–1017. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., et al. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190. Bucher, M. (2007). Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173, 11–26. Buhtz, A., Springer, F., Chappell, L., et al. (2008). Identification and characterization of small RNAs from the phloem of Brassica napus . Plant Journal 53, 739–749. Burleigh, S.H. & Harrison, M.J. (1999). The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiology 119, 241–248. Bustos, R., Castrillo, G., Linhares, F., et al. (2010). A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis . PLoS Genetics 6, e1001102. Carswell, C., Grant, B.R., Theodorou, M.E., et al. (1996). The fungicide phosphonate disrupts the phosphate-starvation response in Brassica nigra seedlings. Plant Physiology 110, 105–110. Carswell, M.C., Grant, B.R., & Plaxton, W.C. (1997). Disruption of the phosphate-starvation response of oilseed rape suspension cells by the fungicide phosphonate. Planta 203, 67–74. Chandrika, N.N.P., Sundaravelpandian, K., Yu, S.-M., et al. (2013). ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis . New Phytologist 198, 709–720. Chapin, F.S. Bieleski, R.L. (1982). Mild phosphorus stress in barley and a related low-phosphorus-adapted barleygrass: Phosphorus fractions and phosphate absorption in relation to growth. Physiologia Plantarum 54, 309–317. Chen, L., Hao, L., Parry, M.A.J., et al. (2014). Progress in TILLING as a tool for functional genomics and improvement of crops. Journal of Integrative Plant Biology 56, 425–443. Chen, Y.-F., Li, L.-Q., Xu, Q., et al. (2009). The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis . Plant Cell 21, 3554–3566. Chen, Z.-H., Nimmo, G.A., Jenkins, G.I., et al. (2007). BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis . Biochemical Journal 405, 191–198. Chevalier, F., Pata, M., Nacry, P., et al. (2003). Effects of phosphate availability on the root system architecture: large-scale analysis of the natural variation between Arabidopsis accessions. Plant, Cell & Environment 26, 1839–1850. Chevalier, F. & Rossignol, M. (2011). Proteomic analysis of Arabidopsis thaliana ecotypes with contrasted root architecture in response to phosphate deficiency. Journal of Plant Physiology 168, 1885–1890. Chin, J.H., Gamuyao, R., Dalid, C., et al. (2011). Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiology 156, 1202–1216. Chiou, T.-J., Aung, K., Lin, S.-I., et al. (2006). Regulation of phosphate homeostasis by microRNA in Arabidopsis . Plant Cell 18, 412–421. Chiou, T.-J. & Lin, S.-I. (2011). Signaling network in sensing phosphate availability in plants. Annual Review of Plant Biology 62, 185–206. Cho, H.-T. & Lee, R.D.W. (2013). Auxin, the organizer of the environmental/hormonal signals for root hair growth. Frontiers in Plant Science 4, 1–7. Cong, L., Ran, F.A., Cox, D., et al. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819–823. Cordell, D., Schmid-Neset, T., White, S., et al. (2009). Preferred future phosphorus scenarios: a framework for meeting long-term phosphorus needs for global food demand. In: K. Ashley, D. Mavinic, & F. Koch (eds.) International Conference on Nutrient Recovery from Wastewater Streams, IWA Publishing, London, UK, pp. 23–43. Czarnecki, O., Yang, J., Weston, D., et al. (2013). A dual role of strigolactones in phosphate acquisition and utilization in plants. International Journal of Molecular Sciences 14, 7681–7701. Czyzewicz, N., Yue, K., Beeckman, T., et al. (2013). Message in a bottle: small signalling peptide outputs during growth and development. Journal of Experimental Botany 64, 5281–5296. Dai, X., Wang, Y., Yang, A., et al. (2012). OsMYB2P-1, an R2R3 MYB transcription factor, Is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiology 159, 169–183. Dalio, R.J.D., Fleischmann, F., Humez, M., et al. (2014). Phosphite protects Fagus sylvatica seedlings towards Phytophthora plurivora via local toxicity, priming and facilitation of pathogen recognition. PLoS ONE 9, 1–10. Danova-Alt, R., Dijkema, C.O.R., De Waard, P., et al. (2008). Transport and compartmentation of phosphite in higher plant cells – kinetic and 31P nuclear magnetic resonance studies. Plant, Cell & Environment 31, 1510–1521. Dasgupta, K., Khadilkar, A.S., Sulpice, R., et al. (2014). Expression of sucrose transporter cDNAs specifically in companion cells enhances phloem loading and long-distance transport of sucrose but leads to an inhibition of growth and the perception of a phosphate limitation. Plant Physiology 165, 715–731. Dawson, C.J. & Hilton, J. (2011). Fertiliser availability in a resource-limited world: production and recycling of nitrogen and phosphorus. Food Policy 36, S14–S22. Deb, S., Sankaranarayanan, S., Wewala, G., et al. (2014). The S-domain receptor kinase AtARK2 and the U-box/ARM-repeat-containing E3 ubiquitin ligase AtPUB9 module mediates lateral root development under phosphate starvation in Arabidopsis . Plant Physiology 165, 1647–1656. Delay, C., Imin, N., & Djordjevic, M.A. (2013). CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. Journal of Experimental Botany 64, 5383–5394. Delhaize, E. & Randall, P.J. (1995). Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana . Plant Physiology 107, 207–213. Delhaize, E., Hebb, D.M., & Ryan, P.R. (2001). Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiology 125, 2059–2067. Den Herder, G.D., Van Isterdael, G., Beeckman, T., et al. (2010). The roots of a new green revolution. Trends in Plant Science 15, 600—607. Devaiah, B.N., Karthikeyan, A.S., & Raghothama, K.G. (2007a). WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis . Plant Physiology 143, 1789–1801. Devaiah, B.N., Nagarajan, V.K., & Raghothama, K.G. (2007b). Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiology 145, 147–159. Devaiah, B.N., Madhuvanthi, R., Karthikeyan, A.S., et al. (2009). Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis . Molecular Plant 2, 43–58. Drew, M.C., He, C.-J., & Morgan, P.W. (1989). Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiology 91, 266–271. Duan, K., Yi, K., Dang, L., Huang, H., et al. (2008). Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant Journal 54, 965–975. Dunoyer, P., Schott, G., Himber, C., et al. (2010). Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912–916. Fife, C.A., Newcomb, W., & Lefebvre, D.D. (1990). The effect of phosphate deprivation on protein synthesis and fixed carbon storage reserves in Brassica nigra suspension cells. Canadian Journal of Botany 68, 1840–1847. Fixen, P.E. & Johnston, A.M. (2012). World fertilizer nutrient reserves: a view to the future. Journal of the Science of Food and Agriculture 92, 1001–1005. Foo, E., Yoneyama, K., Hugill, C., et al. (2013). Strigolactones: internal and external signals in plant symbioses? Plant Signaling & Behavior 8, e23168. Franco-Zorrilla, J.M., Martin, A.C., Solano, R., et al. (2002). Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis . Plant Journal 32, 353–360. Franco-Zorrilla, J.M., Martín, A.C., Leyva, A., et al. (2005). Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiology 138, 847–857. Franco-Zorrilla, J.M., Valli, A., Todesco, M., et al. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics 39, 1033–1037. Franco-Zorrilla, J.M., González, E., Bustos, R., et al. (2004). The transcriptional control of plant responses to phosphate limitation. Journal of Experimental Botany 55, 285–293. Fredeen, A.L., Rao, I.M., & Terry, N. (1989). Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max . Plant Physiology 89, 225–230. Fröhlich, A., Gaupels, F., Sarioglu, H., et al. (2012). Looking deep inside: detection of low-abundance proteins in leaf extracts of Arabidopsis and phloem exudates of pumpkin. Plant Physiology 159, 902–914. Fujii, H., Chiou, T.-J., Lin, S.-I., et al. (2005). A miRNA involved in phosphate-starvation response in Arabidopsis . Current Biology 15, 2038–2043. Funayama-Noguchi, S., Noguchi, K., Yoshida, C., et al. (2011). Two CLE genes are induced by phosphate in roots of Lotus japonicus . Journal of Plant Research 124, 155–163. Gamuyao, R., Chin, J.H., Pariasca-Tanaka, J., et al. (2012). The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488, 535–539. Gao, N., Su, Y., Min, J., Shen, W., et al. (2010). Transgenic tomato overexpressing ath-miR399d has enhanced phosphorus accumulation through increased acid phosphatase and proton secretion as well as phosphate transporters. Plant and Soil 334, 123–136. Gaude, N., Nakamura, Y., Scheible, W.-R., et al. (2008). Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis . Plant Journal 56, 28–39. Gilbert, G.A., Knight, J.D., Vance, C.P., et al. (2000). Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Annals of Botany 85, 921–928. Giots, F., Donaton, M.C.V., & Thevelein, J.M. (2003). Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase A pathway in the yeast Saccharomyces cerevisiae . Molecular Microbiology 47, 1163–1181. Gomez-Roldan, V., Fermas, S., Brewer, P.B., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455, 189–194. Guo, W., Zhao, J., Li, X., et al. (2011). A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant Journal 66, 541–552. Hackenberg, M., Shi, B.-J., Gustafson, P., et al. (2013a). Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biology 13, 1–17. Hackenberg, M., Huang, P.-J., Huang, C.-Y., et al. (2013b). A Comprehensive Expression Profile of microRNAs and other classes of non-coding small RNAs in barley under phosphorous-deficient and -sufficient conditions. DNA Research 20, 109–125. Hamburger, D., Rezzonico, E., MacDonald-Comber Petétot, J., et al. (2002). Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14, 889–902. Hammond, J.P. & White, P.J. (2008). Sucrose transport in the phloem: integrating root responses to phosphorus starvation. Journal of Experimental Botany 59, 93–109. Han, Y.-Y., Zhou, S., Chen, Y., et al. (2014). The involvement of expansins in responses to phosphorus availability in wheat, and its potentials in improving phosphorus efficiency of plants. Plant Physiology and Biochemistry 78, 53–62. He, C.-J., Morgan, P.W., & Drew, M.C. (1992). Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiology 98, 137–142. He, Z., Ma, Z., Brown, K.M., et al. (2005). Assessment of inequality of root hair density in Arabidopsis thaliana using the Gini coefficient: a close look at the effect of phosphorus and its interaction with ethylene. Annals of Botany 95, 287–293. Hewitt, M.M., Carr, J.M., Williamson, C.L., et al. (2005). Effects of phosphate limitation on expression of genes involved in pyrimidine synthesis and salvaging in Arabidopsis . Plant Physiology and Biochemistry 43, 91–99. Ho, C.-H., Lin, S.-H., Hu, H.-C., et al. (2009). CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194. Holsbeeks, I., Lagatie, O., Van Nuland, A., et al. (2004). The eukaryotic plasma membrane as a nutrient-sensing device. Trends in Biochemical Sciences 29, 556–564. Horgan, J.M. & Wareing, P.F. (1980). Cytokinins and the growth responses of seedlings of Betula pendula Roth. and Acer pseudoplatanus L. to nitrogen and phosphorus deficiency. Journal of Experimental Botany 31, 525–532. Hsieh, L.-C., Lin, S.-I., Shih, A.C.-C., et al. (2009). Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151, 2120–2132. Hu, B., Zhu, C., Li, F., Tang, J., et al. (2011). LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiology 156, 1101–1115. Huang, T.-K., Han, C.-L., Lin, S.-I., et al. (2013). Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25, 4044–4060. Hurley, B.A., Tran, H.T., Marty, N.J., et al. (2010). The dual-targeted purple acid phosphatase isozyme AtPAP26 is essential for efficient acclimation of Arabidopsis to nutritional phosphate deprivation. Plant Physiology 153, 1112–1122. Iglesias, J., Trigueros, M., Rojas-Triana, M., et al. (2013). Proteomics identifies ubiquitin–proteasome targets and new roles for chromatin-remodeling in the Arabidopsis response to phosphate starvation. Journal of Proteomics 94, 1–22. Imin, N., Mohd-Radzman, N.A., Ogilvie, H.A., et al. (2013). The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula . Journal of Experimental Botany 64, 5395–5409. Israel, D.W., Rufty, T.W., & Cure, J.D. (1990). Nitrogen and phosphorus nutritional interactions in a CO2 enriched environment. Journal of Plant Nutrition 13, 1419–1433. Jain, A., Poling, M.D., Karthikeyan, A.S., et al. (2007). Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis . Plant Physiology 144, 232–247. Jiang, C., Gao, X., Liao, L., et al. (2007). Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis . Plant Physiology 145, 1460–1470. Kanno, Y., Jikumaru, Y., Hanada, A., et al. (2010). Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant and Cell Physiology 51, 1988–2001. Kant, S., Peng, M., & Rothstein, S.J. (2011). Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis . PLoS Genetics 7, e1002021. Karthikeyan, A., Varadarajan, D., Jain, A., et al. (2007). Phosphate starvation responses are mediated by sugar signaling in Arabidopsis . Planta 225, 907–918. Kehr, J. & Buhtz, A. (2008). Long distance transport and movement of RNA through the phloem. Journal of Experimental Botany 59, 85–92. Kim, E.-D. & Sung, S. (2012). Long noncoding RNA: unveiling hidden layer of gene regulatory networks. Trends in Plant Science 17, 16–21. Kim, H.-J., Lynch, J.P., & Brown, K.M. (2008). Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant, Cell & Environment 31, 1744–1755. Köck, M., Stenzel, I., & Zimmer, A. (2006). Tissue-specific expression of tomato ribonuclease LX during phosphate starvation-induced root growth. Journal of Experimental Botany 57, 3717–3726. Kohlen, W., Charnikhova, T., Liu, Q., et al. (2011). Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis . Plant Physiology 155, 974–987. Kretzschmar, T., Kohlen, W., Sasse, J., et al. (2012). A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483, 341–344. Krouk, G., Lacombe, B., Bielach, A., et al. (2010). Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell 18, 927–937. Kuiper, D., Schuit, J., & Kuiper, P.C. (1988). Effects of internal and external cytokinin concentrations on root growth and shoot to root ratio of Plantago major ssp. Pleiosperma at different nutrient conditions. Plant and Soil 111, 231–236. Lai, F., Thacker, J., Li, Y., & Doerner, P. (2007). Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis . Plant Journal 50, 545–556. Lambers, H., Finnegan, P.M., Laliberte, E., et al. (2011). Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiology 156, 1058–1066. Lan, P., Li, W., & Schmidt, W. (2012). Complementary proteome and transcriptome profiling in phosphate-deficient Arabidopsis roots reveals multiple levels of gene regulation. Molecular & Cellular Proteomics 11, 1156–1166. Lei, M., Zhu, C., Liu, Y., et al. (2011a). Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis . New Phytologist 189, 1084–1095. Lei, M., Liu, Y., Zhang, B., et al. (2011b). Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis . Plant Physiology 156, 1116–1130. Li, D., Zhu, H., Liu, K., et al. (2002). Purple acid phosphatases of Arabidopsis thaliana. Comparative analysis and differential regulation by phosphate deprivation. The Journal of Biological Chemistry 277, 27772–27781. Li, Z., Gao, Q., Liu, Y., et al. (2011). Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta 233, 1129–1143. Lim, S., Borza, T., Peters, R.D., et al. (2013). Proteomics analysis suggests broad functional changes in potato leaves triggered by phosphites and a complex indirect mode of action against Phytophthora infestans . Journal of Proteomics 93, 207–223. Lin, S.-I., Chiang, S.-F., Lin, W.-Y., et al. (2008). Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiology 147, 732–746. Lin, S.-I., Santi, C., Jobet, E., et al. (2010). Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant and Cell Physiology 51, 2119–2131. Lin, W.-Y., Huang, T.-K., & Chiou, T.-J. (2013). NITROGEN LIMITATION ADAPTATION, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis . Plant Cell 25, 4061–4074. Liu, B., Kanazawa, A., Matsumura, H., et al. (2008). Genetic redundancy in soybean photoresponses associated with duplication of the phytochrome A gene. Genetics 180, 995–1007. Liu, H., Yang, H., Wu, C., et al. (2009). Overexpressing HRS1 confers hypersensitivity to low phosphate-elicited inhibition of primary root growth in Arabidopsis thaliana . Journal of Integrative Plant Biology 51, 382–392. Liu, J.-Q., Allan, D., & Vance, C. (2010). Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Molecular Plant 3, 428–437. Liu, J., Samac, D.A., Bucciarelli, B., et al. (2005). Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant Journal 41, 257–268. Liu, T.-Y., Aung, K., Tseng, C.-Y., et al. (2011). Vacuolar Ca2+/H+ transport activity is required for systemic phosphate homeostasis involving shoot-to-root signaling in Arabidopsis . Plant Physiology 156, 1176–1189. Liu, T.-Y., Huang, T.-K., Tseng, C.-Y., et al. (2012). PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis . Plant Cell 24, 2168–2183. Lloyd, J.C. & Zakhleniuk, O.V. (2004). Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3 . Journal of Experimental Botany 55, 1221–1230. Lopez-Arredondo, D.L. & Herrera-Estrella, L. (2012). Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system. Nature Biotechnology 30, 889–893. López-Arredondo, D.L., Leyva-González, M.A., González-Morales, S.I., et al. (2014). Phosphate nutrition: improving low-phosphate tolerance in crops. Annual Review of Plant Biology 65, 95–1
Publication Year: 2015
Publication Date: 2015-04-14
Language: en
Type: other
Indexed In: ['crossref']
Access and Citation
Cited By Count: 23
AI Researcher Chatbot
Get quick answers to your questions about the article from our AI researcher chatbot