Sulfur Deficiency Increases Phosphate Accumulation, Uptake, and Transport in Arabidopsis thaliana

1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

Long, S.; Kahn, M.; Seefeldt, L.; Tsay, Y.; Kopriva, S. Nitrogen and sulfur. In Biochemistry and Molecular Biology

of Plants; Buchanan, B.B., Gruissem, W., Jones, R.L., Eds.; WILEY: Blackwell, NJ, USA, 2015; pp. 746–768.

Plaxton, W.C.; Tran, H.T. Metabolic adaptations of phosphate-starved plants. Plant Physiol. 2011, 156,

1006–1015. [CrossRef]

Ticconi, C.A.; Abel, S. Short on phosphate: Plant surveillance and countermeasures. Trends Plant Sci. 2004, 9,

548–555. [CrossRef] [PubMed]

Shen, J.; Yuan, L.; Zhang, J.; Li, H.; Bai, Z.; Chen, X.; Zhang, W.; Zhang, F. Phosphorus dynamics: From soil to

plant. Plant Physiol. 2011, 156, 997–1005. [CrossRef] [PubMed]

Poirier, Y.; Bucher, M. Phosphate transport and homeostasis in Arabidopsis. Arab. Book 2002, 1, e0024.

[CrossRef] [PubMed]

Saito, K. Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol. 2004, 136, 2443–2450.

[CrossRef]

Takahashi, H.; Kopriva, S.; Giordano, M.; Saito, K.; Hell, R. Sulfur assimilation in photosynthetic organisms:

Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 2011,

62, 157–184. [CrossRef]

Tripathy, B.C.; Sherameti, I.; Oelmüller, R. Siroheme. Plant Signal. Behav. 2010, 5, 14–20. [CrossRef]

Leustek, T. Sulfate metabolism. Arab. Book 2002, 1, e0017. [CrossRef]

Nikiforova, V.J.; Kopka, J.; Tolstikov, V.; Fiehn, O.; Hopkins, L.; Hawkesford, M.J.; Hesse, H.; Hoefgen, R.

Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of

Arabidopsis plants. Plant Physiol. 2005, 138, 304–318. [CrossRef]

Maruyama-Nakashita, A.; Ohkama-Ohtsu, N. Chapter 13 Sulfur assimilation and glutathione metabolism in

plants. In Glutathione in Plant Growth, Development, and Stress Tolerance; Springer: New York, NY, USA, 2017;

pp. 287–308.

Stigter, K.; Plaxton, W.; Stigter, K.A.; Plaxton, W.C. Molecular Mechanisms of Phosphorus Metabolism and

Transport during Leaf Senescence. Plants 2015, 4, 773–798. [CrossRef]

Misson, J.; Raghothama, K.G.; Jain, A.; Jouhet, J.; Block, M.A.; Bligny, R.; Ortet, P.; Creff, A.; Somerville, S.;

Rolland, N.; et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips

determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. USA 2005, 102, 11934–11939.

[CrossRef]

Rouached, H.; Secco, D.; Arpat, B.; Poirier, Y. The transcription factor PHR1 plays a key role in the regulation

of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biol. 2011, 11, 19. [CrossRef]

[PubMed]

Yu, B.; Xu, C.; Benning, C. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in

phosphate-limited growth. Proc. Natl. Acad. Sci. USA 2002, 99, 5732–5737. [CrossRef] [PubMed]

Okazaki, Y.; Otsuki, H.; Narisawa, T.; Kobayashi, M.; Sawai, S.; Kamide, Y.; Kusano, M.; Aoki, T.; Hirai, M.Y.;

Saito, K. A new class of plant lipid is essential for protection against phosphorus depletion. Nat. Commun.

2013, 4, 1510. [CrossRef] [PubMed]

Okazaki, Y.; Shimojima, M.; Sawada, Y.; Toyooka, K.; Narisawa, T.; Mochida, K.; Tanaka, H.; Matsuda, F.;

Hirai, A.; Hirai, M.Y.; et al. A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the

committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 2009, 21, 892–909. [CrossRef]

[PubMed]

Shimojima, M. Biosynthesis and functions of the plant sulfolipid. Prog. Lipid Res. 2011, 50, 234–239.

[CrossRef] [PubMed]

Liang, G.; Ai, Q.; Yu, D. Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis.

Sci. Rep. 2015, 5, 11813. [CrossRef]

Hsieh, L.-C.; Lin, S.-I.; Shih, A.C.-C.; Chen, J.-W.; Lin, W.-Y.; Tseng, C.-Y.; Li, W.-H.; Chiou, T.-J. Uncoveing small

RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 2009,

151, 2120–2132. [CrossRef]

Hirsch, J.; Marin, E.; Floriani, M.; Chiarenza, S.; Richaud, P.; Nussaume, L.; Thibaud, M.C. Phosphate

deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 2006, 88, 1767–1771.

[CrossRef]

Int. J. Mol. Sci. 2020, 21, 2971

22.

23.

24.

25.

26.

27.

28.

29.

30.

31.

32.

33.

34.

35.

36.

37.

38.

39.

40.

41.

13 of 15

Nocito, F.F.; Pirovano, L.; Cocucci, M.; Sacchi, G.A. Cadmium-induced sulfate uptake in maize roots.

Plant Physiol. 2002, 129, 1872–1879. [CrossRef]

Kandlbinder, A.; Finkemeier, I.; Wormuth, D.; Hanitzsch, M.; Dietz, K.-J. The antioxidant status of

photosynthesizing leaves under nutrient deficiency: Redox regulation, gene expression and antioxidant

activity in Arabidopsis thaliana. Physiol. Plant. 2004, 120, 63–73. [CrossRef] [PubMed]

Guo, B.; Jin, Y.; Wussler, C.; Blancaflor, E.B.; Motes, C.M.; Versaw, W.K. Functional analysis of the Arabidopsis

PHT4 family of intracellular phosphate transporters. New Phytol. 2008, 177, 889–898. [CrossRef] [PubMed]

Nussaume, L.; Kanno, S.; Javot, H.; Marin, E.; Pochon, N.; Ayadi, A.; Nakanishi, T.M.; Thibaud, M.C.

Phosphate import in plants: Focus on the PHT1 transporters. Front. Plant Sci. 2011, 2, 83. [CrossRef]

Kisko, M.; Shukla, V.; Kaur, M.; Bouain, N.; Chaiwong, N.; Lacombe, B.; Pandey, A.; Rouached, H.; Kisko, M.;

Shukla, V.; et al. Phosphorus transport in Arabidopsis and Wheat: Emerging strategies to improve P pool in

seeds. Agriculture 2018, 8, 27. [CrossRef]

Misson, J.; Thibaud, M.-C.; Bechtold, N.; Raghothama, K.; Nussaume, L. Transcriptional regulation and

functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate

uptake in phosphate deprived plants. Plant Mol. Biol. 2004, 55, 727–741. [CrossRef] [PubMed]

Shin, H.; Shin, H.-S.; Dewbre, G.R.; Harrison, M.J. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play

a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 2004, 39,

629–642. [CrossRef] [PubMed]

Mudge, S.R.; Rae, A.L.; Diatloff, E.; Smith, F.W. Expression analysis suggests novel roles for members of the

Pht1 family of phosphate transporters in Arabidopsis. Plant J. 2002, 31, 341–353. [CrossRef] [PubMed]

Nagarajan, V.K.; Jain, A.; Poling, M.D.; Lewis, A.J.; Raghothama, K.G.; Smith, A.P. Arabidopsis Pht1;5

mobilizes phosphate between source and sink organs and influences the interaction between phosphate

homeostasis and ethylene signaling. Plant Physiol. 2011, 156, 1149–1163. [CrossRef]

Remy, E.; Cabrito, T.R.; Batista, R.A.; Teixeira, M.C.; Sá-Correia, I.; Duque, P. The Pht1;9 and Pht1;8 transporters

mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation.

New Phytol. 2012, 195, 356–371. [CrossRef]

Lapis-Gaza, H.R.; Jost, R.; Finnegan, P.M. Arabidopsis Phosphate Transportar1 genes PHT1;8 and PHT1;9

are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol. 2014, 14, 334. [CrossRef]

Poirier, Y.; Thoma, S.; Somerville, C.; Schiefelbein, J. Mutant of Arabidopsis deficient in xylem loading of

phosphate. Plant Physiol. 1991, 97, 1087–1093. [CrossRef] [PubMed]

Hamburger, D.; Rezzonico, E.; MacDonald-Comber Petétot, J.; Somerville, C.; Poirier, Y. Identification and

characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 2002,

14, 889–902. [CrossRef] [PubMed]

Wang, Y.; Ribot, C.; Rezzonico, E.; Poirier, Y. Structure and expression profile of the Arabidopsis PHO1

gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol. 2004, 135, 400–411.

[CrossRef] [PubMed]

López-Bucio, J.; Cruz-Ramírez, A.; Herrera-Estrella, L. The role of nutrient availability in regulating root

architecture. Curr. Opin. Plant Biol. 2003, 6, 280–287. [CrossRef]

Kimura, Y.; Ushiwatari, T.; Suyama, A.; Tominaga-Wada, R.; Wada, T.; Maruyama-Nakashita, A. Contribution of

root hair development to sulfate uptake in Arabidopsis. Plants 2019, 8, 106. [CrossRef]

Maruyama-Nakashita, A. Metabolic changes sustain the plant life in low-sulfur environments. Curr. Opin.

Plant Biol. 2017, 39, 144–151. [CrossRef]

Maruyama-Nakashita, A.; Inoue, E.; Watanabe-Takahashi, A.; Yamaya, T.; Takahashi, H. Transcriptome profiling

of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic

pathways. Plant Physiol. 2003, 132, 597–605. [CrossRef]

Kataoka, T.; Hayashi, N.; Yamaya, T.; Takahashi, H. Root-to-shoot transport of sulfate in Arabidopsis.

Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root

vasculature. Plant Physiol. 2004, 136, 4198–4204.

Hirai, M.Y.; Klein, M.; Fujikawa, Y.; Yano, M.; Goodenowe, D.B.; Yamazaki, Y.; Kanaya, S.; Nakamura, Y.;

Kitayama, M.; Suzuki, H.; et al. Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis

by integration of metabolomics and transcriptomics. J. Biol. Chem. 2005, 280, 25590–25595. [CrossRef]

Int. J. Mol. Sci. 2020, 21, 2971

42.

43.

44.

45.

46.

47.

48.

49.

50.

51.

52.

53.

54.

55.

56.

57.

58.

14 of 15

Aarabi, F.; Kusajima, M.; Tohge, T.; Konishi, T.; Gigolashvili, T.; Takamune, M.; Sasazaki, Y.; Watanabe, M.;

Nakashita, H.; Fernie, A.R.; et al. Sulfur deficiency–induced repressor proteins optimize glucosinolate

biosynthesis in plants. Sci. Adv. 2016, 2, e1601087. [CrossRef]

Zhang, L.; Kawaguchi, R.; Morikawa-Ichinose, T.; Allahham, A.; Kim, S.-J.; Maruyama-Nakashita, A.

Sulfur deficiency-induced glucosinolate catabolism attributed to two β-Glucosidases, BGLU28 and BGLU30,

is required for plant growth maintenance under sulfur deficiency. Plant Cell Physiol. 2020, 61, 803–813.

[CrossRef]

Maruyama-Nakashita, A.; Nakamura, Y.; Tohge, T.; Saito, K.; Takahashi, H. Arabidopsis SLIM1 is a central

transcriptional regulator of plant sulfur response and metabolism. Plant Cell 2006, 18, 3235–3251. [CrossRef]

[PubMed]

Sakuraba, Y.; Kanno, S.; Mabuchi, A.; Monda, K.; Iba, K.; Yanagisawa, S. A phytochrome-B-mediated

regulatory mechanism of phosphorus acquisition. Nat. Plants 2018, 4, 1089–1101. [CrossRef] [PubMed]

Kanno, S.; Cuyas, L.; Javot, H.; Bligny, R.; Gout, E.; Dartevelle, T.; Hanchi, M.; Nakanishi, T.M.; Thibaud, M.-C.;

Nussaume, L. Performance and limitations of phosphate wuantification: Guidelines for plant biologists.

Plant Cell Physiol. 2016, 57, 690–706. [CrossRef] [PubMed]

Rubio, V.; Linhares, F.; Solano, R.; Martín, A.C.; Iglesias, J.; Leyva, A.; Paz-Ares, J. A conserved MYB

transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular

algae. Genes Dev. 2001, 15, 2122–2133. [CrossRef] [PubMed]

Bustos, R.; Castrillo, G.; Linhares, F.; Puga, M.I.; Rubio, V.; Pérez-Pérez, J.; Solano, R.; Leyva, A.; Paz-Ares, J.

A central regulatory system largely controls transcriptional activation and repression responses to phosphate

starvation in Arabidopsis. PLoS Genet. 2010, 6, e1001102. [CrossRef] [PubMed]

Maruyama-Nakashita, A.; Nakamura, Y.; Yamaya, T.; Takahashi, H. A novel regulatory pathway of sulfate

uptake in Arabidopsis roots: Implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation.

Plant J. 2004, 38, 779–789. [CrossRef]

Lin, W.Y.; Huang, T.K.; Chiou, T.J. Nitrogen Limitation Adaptation, a target of MicroRNA827,

mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate

homeostasis in Arabidopsis. Plant Cell 2013, 25, 4061–4074. [CrossRef]

Chen, J.; Wang, Y.; Wang, F.; Yang, J.; Gao, M.; Li, C.; Liu, Y.; Liu, Y.; Yamaji, N.; Ma, J.F.; et al. The rice CK2

kinase regulates trafficking of phosphate transporters in response to phosphate levels. Plant Cell 2015, 27,

711–723. [CrossRef]

Yue, W.; Ying, Y.; Wang, C.; Zhao, Y.; Dong, C.; Whelan, J.; Shou, H. OsNLA1, a RING-type ubiquitin ligase,

maintains phosphate homeostasis in Oryza sativa via degradation of phosphate transporters. Plant J. 2017, 90,

1040–1051. [CrossRef]

Bari, R.P.; Pant, B.D.; Stitt, M.; Scheible, W.R. PHO2, microRNA399 and PHR1 define a phosphate signalling

pathway in plants. Plant Physiol. 2006, 141, 988–999. [CrossRef] [PubMed]

Liu, T.-Y.; Huang, T.-K.; Tseng, C.-Y.; Lai, Y.-S.; Lin, S.-I.; Lin, W.-Y.; Chen, J.-W.; Chiou, T.-J. PHO2-dependent

degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 2012, 24, 2168–2183.

[CrossRef]

Huang, T.-K.; Han, C.-L.; Lin, S.-I.; Chen, Y.-J.; Tsai, Y.-C.; Chen, Y.-R.; Chen, J.-W.; Lin, W.-Y.; Chen, P.-M.;

Liu, T.-Y.; et al. Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2

by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 2013, 25, 4044–4060. [CrossRef]

[PubMed]

Chang, M.X.; Gu, M.; Xia, Y.W.; Dai, X.L.; Chang, R.D.; Zhang, J.; Wang, S.C.; Qu, H.Y.; Yamaji, N.; Ma, J.F.; et al.

OsPHT1;3 mediates uptake, translocation, and remobilization of phosphate under extremely low phosphate

regimes. Plant Physiol. 2019, 179, 656–670. [CrossRef] [PubMed]

Pedersen, B.P.; Kumar, H.; Waight, A.B.; Risenmay, A.J.; Roe-Zurz, Z.; Chau, B.H.; Schlessinger, A.; Bonomi, M.;

Harries, W.; Sali, A.; et al. Crystal structure of a eukaryotic phosphate transporter. Nature 2013, 496, 533–536.

[CrossRef] [PubMed]

Chiou, T.J.; Liu, H.; Harrison, M.J. The spatial expression patterns of a phosphate transporter (MtPT1) from

Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J. 2001, 25, 281–293.

[CrossRef] [PubMed]

Int. J. Mol. Sci. 2020, 21, 2971

59.

60.

61.

62.

63.

64.

65.

66.

67.

68.

69.

70.

71.

72.

73.

15 of 15

Fontenot, E.B.; DiTusa, S.F.; Kato, N.; Olivier, D.M.; Dale, R.; Lin, W.Y.; Chiou, T.J.; Macnaughtan, M.A.;

Smith, A.P. Increased phosphate transport of Arabidopsis thaliana Pht1;1 by site-directed mutagenesis of

tyrosine 312 may be attributed to the disruption of homomeric interactions. Plant Cell Environ. 2015, 38,

2012–2022. [CrossRef]

Gilroy, S.; Jones, D.L. Through form to function: Root hair development and nutrient uptake. Trends Plant Sci.

2000, 5, 56–60. [CrossRef]

Ma, Z.; Bielenberg, D.G.; Brown, K.M.; Lynch, J.P. Regulation of root hair density by phosphorus availability

in Arabidopsis thaliana. Plant Cell Environ. 2001, 24, 459–467. [CrossRef]

Wege, S.; Khan, G.A.; Jung, J.Y.; Vogiatzaki, E.; Pradervand, S.; Aller, I.; Meyer, A.J.; Poirier, Y. The EXS

Domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal.

Plant Physiol. 2016, 170, 385–400. [CrossRef]

Vogiatzaki, E.; Baroux, C.; Jung, J.Y.; Poirier, Y. PHO1 exports phosphate from the chalazal seed coat to the

embryo in developing Arabidopsis seeds. Curr. Biol. 2017, 27, 2893–2900. [CrossRef] [PubMed]

Rouached, H.; Arpat, A.B.; Poirier, Y. Regulation of phosphate starvation responses in plants: Signaling players

and cross-talks. Mol. Plant 2010, 3, 288–299. [CrossRef] [PubMed]

Młodzinska,

E.; Zboinska,

M. Phosphate uptake and allocation—A closer look at arabidopsis thaliana L. and

Oryza sativa L. Front. Plant Sci. 2016, 7, 1198. [CrossRef] [PubMed]

Fujiwara, T.; Lessard, P.A.; Beachy, R.N. Seed-specific repression of GUS activity in tobacco plants by antisense

RNA. Plant Mol. Biol. 1992, 20, 1059–1069. [CrossRef]

Hirai, M.Y.; Fujiwara, T.; Chino, M.; Naito, S. Effects of sulfate concentrations on the expression of a soybean

seed storage protein gene and its reversibility in transgenic Arabidopsis thaliana. Plant Cell Physiol. 1995, 36,

1331–1339. [PubMed]

Yamaguchi, C.; Takimoto, Y.; Ohkama-Ohtsu, N.; Hokura, A.; Shinano, T.; Nakamura, T.; Suyama, A.;

Maruyama-Nakashita, A. Effects of cadmium treatment on the uptake and translocation of sulfate in

Arabidopsis thaliana. Plant Cell Physiol. 2016, 57, 2353–2366. [CrossRef]

Murphy, J.; Riley, J.P. A modified single solution method for the determination of phosphate in natural

waters. Anal. Chim. Acta 1962, 27, 31–36. [CrossRef]

Puga, M.I.; Mateos, I.; Charukesi, R.; Wang, Z.; Franco-Zorrilla, J.M.; De Lorenzo, L.; Irigoyen, M.L.;

Masiero, S.; Bustos, R.; Rodríguez, J.; et al. SPX1 is a phosphate-dependent inhibitor of Phosphate Starvation

Response 1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 2014, 111, 14947–14952. [CrossRef]

Stefanovic, A.; Ribot, C.; Rouached, H.; Wang, Y.; Chong, J.; Belbahri, L.; Delessert, S.; Poirier, Y. Members of

the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are

regulated by phosphate deficiency via distinct pathways. Plant J. 2007, 50, 982–994. [CrossRef]

Valvekens, D.; Van Montagu, M.; Van Lijsebettens, M. Agrobacterium tumefaciens-mediated transformation

of Arabidopsis thaliana root explants by using kanamycin selection. Proc. Natl. Acad. Sci. USA 1988, 85,

5536–5540. [CrossRef]

Horie, T.; Motoda, J.; Kubo, M.; Yang, H.; Yoda, K.; Horie, R.; Chan, W.-Y.; Leung, H.-Y.; Hattori, K.;

Konomi, M.; et al. Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from

xylem vessels to xylem parenchyma cells. Plant J. 2005, 44, 928–938. [CrossRef] [PubMed]

© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access

article distributed under the terms and conditions of the Creative Commons Attribution

(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

...