Advertisement

Molecular Genetics and Genomics

, Volume 294, Issue 1, pp 159–175 | Cite as

Tissue-specific transcriptomic profiling of Plantago major provides insights for the involvement of vasculature in phosphate deficiency responses

  • Jing Huang
  • Zhiqiang Huang
  • Xiangjun Zhou
  • Chao Xia
  • Muhammad Imran
  • Shujuan Wang
  • Congshan Xu
  • Manrong Zha
  • Yan Liu
  • Cankui ZhangEmail author
Original Article

Abstract

The vasculature of higher plants is important with transport of both nutrient and information molecules. To understand the correspondence of this tissue in molecular responses under phosphate (Pi) deficiency, Plantago major, a model plant for vasculature biology study, was chosen in our analysis. After RNA-Seq and de novo transcriptome assembly of 24 libraries prepared from the vasculature of P. major, 37,309 unigenes with a mean length of 1571 base pairs were obtained. Upon 24 h of Pi deficiency, 237 genes were shown to be differentially expressed in the vasculature of P. major. Among these genes, only 27 have been previously identified to be specifically expressed in the vasculature tissues in other plant species. Temporal expression of several marker genes associated with Pi deficiency showed that the time period of first 24 h is at the beginning stage of more dynamic expression patterns. In this study, we found several physiological processes, e.g., “phosphate metabolism and remobilization”, “sucrose metabolism, loading and synthesis”, “plant hormone metabolism and signal transduction”, “transcription factors”, and “metabolism of other minerals”, were mainly involved in early responses to Pi deficiency in the vasculature. A number of vasculature genes with promising roles in Pi deficiency adaptation have been identified and deserve further functional characterization. This study clearly demonstrated that plant vasculature is actively involved in Pi deficiency responses and understanding of this process may help to create plants proficient to offset Pi deficiency.

Keywords

Plantago major Vasculature RNA-Seq De novo assembly Phosphate deficiency 

Abbreviations

EST

Expressed sequence tag

FPKM

Fragments per kilobase per transcript per million mapped reads

NR

NCBI non-redundant protein sequences

COG

Clusters of Orthologous Groups of proteins

KEGG

Kyoto Encyclopedia of Genes and Genomes

GO

Gene ontology

Pfam

Protein family

Swiss-Prot

A manually annotated and reviewed protein sequence database

DEG

Differentially expressed gene

Notes

Acknowledgements

We appreciate the technical support from the Purdue Genomics Core Facility Center for RNA-sEq. We are grateful to Dr. Na Liu for critical comments on the manuscript.

Author contributions

CZ and JH conceived and designed the experiments; JH, CX, MZ, SW, CX, IM and YL prepared Plantago major plants and constructed libraries; JH and XZ conducted GUS staining experiment in Arabidopsis; JH performed quantitative real-time PCR; ZH and JH performed bioinformatic analysis; JH and CZ wrote the manuscript; CZ, XZ and IM revised and finalized the manuscript.

Funding

This study was supported by the Purdue Center for Plant Biology Seed Grant (2018).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Data availability

The transcriptomic datasets are available in NCBI with Accession Number SRR6488353 to SRR6488376. This Transcriptome Shotgun Assembly project has been deposited at DDBJ/EMBL/GenBank under the accession GGVT00000000. The version described in this paper is the first version, GGVT01000000.

Supplementary material

438_2018_1496_MOESM1_ESM.docx (14 kb)
Supplementary file 1: Table S1 Statistical analysis of RNA-Seq data. (DOCX 15 kb) (DOCX 14 KB)
438_2018_1496_MOESM2_ESM.xlsx (5.2 mb)
Supplementary file 2: Table S2 Read count numbers and NR annotation of all unigenes. (XLSX 5280 kb) (XLSX 5279 KB)
438_2018_1496_MOESM3_ESM.docx (82 kb)
Supplementary file 3: Fig. S1 Sequence length distribution of transcripts and unigenes assembled from the illumina-sequenced reads. The y-axis indicated the number of transcripts or unigenes in different ranges of sequence length. The x-axis indicated different ranges of sequence length. (DOCX 82 kb) (DOCX 81 KB)
438_2018_1496_MOESM4_ESM.docx (13 kb)
Supplementary file 4: Table S3 Summary of the functional annotation of assembled unigenes. (DOCX 13 kb) (DOCX 12 KB)
438_2018_1496_MOESM5_ESM.docx (283 kb)
Supplementary file 5: Fig. S2 Histogram of GO (gene ontology) classifications of assembled unigenes for P. major vasculature. The unigenes are classified into three main categories: biological process, cellular component and molecular function. For each category, the nine highest GO terms were listed and the rest of the other GO terms are combined as “others”. The y-axis indicated the number of unigenes in different categories. The x-axis indicated different sub-categories of unigenes in each main category. (DOCX 283 kb) (DOCX 282 KB)
438_2018_1496_MOESM6_ESM.docx (22 kb)
Supplementary file 6: Fig. S3 KEGG pathway classifications of assembled unigenes associated with P. major vasculature. The top 20 most enriched pathways were listed to demonstrate the major physiological processes in P. major vasculature. The y-axis indicated different pathways. The x-axis indicated the number of unigenes involved in these pathways. (DOCX 23 kb) (DOCX 22 KB)
438_2018_1496_MOESM7_ESM.xlsx (21 kb)
Supplementary file 7: Table S4 All differentially upregulated genes in P. major vasculature under phosphate deficiency. (XLSX 22 kb) (XLSX 21 KB)
438_2018_1496_MOESM8_ESM.xlsx (23 kb)
Supplementary file 8: Table S5 All differentially downregulated genes in P. major vasculature under phosphate deficiency. (XLSX 23 kb) (XLSX 22 KB)
438_2018_1496_MOESM9_ESM.docx (15 kb)
Supplementary file 9: Table S6 Differentially expressed genes that have been indicated to be specifically expressed in the vasculature in previous studies. (DOCX 15 kb) (DOCX 14 KB)
438_2018_1496_MOESM10_ESM.docx (13 kb)
Supplementary file 10: Table S7 Primer sequences for quantitative real time PCR. (DOCX 13 kb) (DOCX 12 KB)

References

  1. Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8CrossRefGoogle Scholar
  2. An H, Roussot C, Suarez-Lopez P, Corbesier L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131(15):3615–3626CrossRefGoogle Scholar
  3. Aparicio-Fabre R, Guillén G, Loredo M, Arellano J, Valdés-López O, Ramírez M, Íñiguez LP, Panzeri D, Castiglioni B, Cremonesi P (2013) Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency. BMC Plant Biol 13(1):26CrossRefGoogle Scholar
  4. Avila C, Perez-Rodriguez J, Canovas FM (2006) Molecular characterization of a receptor-like protein kinase gene from pine (Pinus sylvestris L.). Planta 224(1):12–19CrossRefGoogle Scholar
  5. Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4(3):377–394CrossRefGoogle Scholar
  6. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141(3):988–999CrossRefGoogle Scholar
  7. Bozzo GG, Raghothama KG, Plaxton WC (2004) Structural and kinetic properties of a novel purple acid phosphatase from phosphate-starved tomato (Lycopersicon esculentum) cell cultures. Biochem J 377(2):419–428CrossRefGoogle Scholar
  8. Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64CrossRefGoogle Scholar
  9. Burleigh SH, Harrison MJ (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 119(1):241–248CrossRefGoogle Scholar
  10. Chen ZH, Nimmo GA, Jenkins GI, Nimmo HG (2007) BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J 405(1):191–198CrossRefGoogle Scholar
  11. Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21(11):3554–3566CrossRefGoogle Scholar
  12. Cheng Y, Zhou W, Peters C, Li M, Wang X, Huang J (2011a) Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation. Plant J 66(5):781–795CrossRefGoogle Scholar
  13. Cheng L, Bucciarelli B, Liu J, Zinn K, Miller S, Patton-Vogt J, Allan D, Shen J, Vance CP (2011b) White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiol 156(3):1131–1148CrossRefGoogle Scholar
  14. Chevalier F, Nieminen K, Sanchez-Ferrero JC, Rodriguez ML, Chagoyen M, Hardtke CS, Cubas P (2014) Strigolactone promotes degradation of DWARF14, an alpha/beta hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26(3):1134–1150CrossRefGoogle Scholar
  15. Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206CrossRefGoogle Scholar
  16. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743CrossRefGoogle Scholar
  17. Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Change 19(2):292–305CrossRefGoogle Scholar
  18. Crafts AS (1932) Phloem anatomy, exudation, and transport of organic nutrients in cucurbits. Plant Physiol 7(2):i4CrossRefGoogle Scholar
  19. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143(4):1789–1801CrossRefGoogle Scholar
  20. Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54(6):965–975CrossRefGoogle Scholar
  21. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144(1):197–205CrossRefGoogle Scholar
  22. Esau K (1973) Comparative structure of companion cells and phloem parenchyma cells in Mimosa pudica L. Ann Bot 37(3):625–632CrossRefGoogle Scholar
  23. Essigmann B, Güler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95(4):1950–1955CrossRefGoogle Scholar
  24. Facchini PJ, Luca VD (1995) Phloem-specific expression of tyrosine/dopa decarboxylase genes and the biosynthesis of isoquinoline alkaloids in Opium Poppy. Plant Cell 7:1811–1821CrossRefGoogle Scholar
  25. Fisher DB, Frame JM (1984) A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161:385–393CrossRefGoogle Scholar
  26. Fukuda A, Okada Y, Suzui N, Fujiwara T, Yoneyama T, Hayashi H (2004) Cloning and characterization of the gene for a phloem-specific glutathione S-transferase from rice leaves. Physiol Plant 120(4):595–602CrossRefGoogle Scholar
  27. Gallie DR, Geisler-Lee J, Chen J, Jolley B (2009) Tissue-specific expression of the ethylene biosynthetic machinery regulates root growth in maize. Plant Mol Biol 69:195–211CrossRefGoogle Scholar
  28. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma F, Birren B, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652CrossRefGoogle Scholar
  29. Grunewald W, Vanholme B, Pauwels L, Plovie E, Inze D, Gheysen G, Goossens A (2009) Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep 10(8):923–928CrossRefGoogle Scholar
  30. Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22(21):2032–2036CrossRefGoogle Scholar
  31. Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59(1):93–109CrossRefGoogle Scholar
  32. Hir LR, Sorin C, Chakraborti D, Moritz T, Schaller H, Tellier F, Robert S, Morin H, Bako L, Bellini C (2013) ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis. Plant J 76(5):811–824CrossRefGoogle Scholar
  33. Hirsch J, Marin E, Floriani M, Chiarenza S, Richaud P, Nussaume L, Thibaud MC (2006) Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 88(11):1767–1771CrossRefGoogle Scholar
  34. Huang C, Barker SJ, Langridge P, Smith FW, Graham RD (2000) Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol 124(1):415–422CrossRefGoogle Scholar
  35. Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Biol 47(1):431–444CrossRefGoogle Scholar
  36. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907CrossRefGoogle Scholar
  37. Kameoka H, Dun EA, Lopez-Obando M, Brewer PB, de Saint Germain A, Rameau C, Beveridge CA, Kyozuka J (2016) Phloem transport of the receptor DWARF14 protein is required for full function of strigolactones. Plant Physiol 172(3):1844–1852CrossRefGoogle Scholar
  38. Khadilkar AS, Yadav UP, Salazar C, Shulaev V, Paez-Valencia J, Pizzio GA, Gaxiola RA, Ayre BG (2016) Constitutive and companion cell-specific overexpression of AVP1, encoding a proton-pumping pyrophosphatase, enhances biomass accumulation, phloem loading, and long-distance transport. Plant Physiol 170(1):401–414CrossRefGoogle Scholar
  39. Khan JA, Wang Q, Sjolund RD, Schulz A, Thompson GA (2007) An early nodulin-like protein accumulates in the sieve element plasma membrane of Arabidopsis. Plant Physiol 143(4):1576–1589CrossRefGoogle Scholar
  40. Khan GA, Vogiatzaki E, Glauser G, Poirier Y (2016) Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory. Plant Physiol 171(1):632–644CrossRefGoogle Scholar
  41. King RW, Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103CrossRefGoogle Scholar
  42. Klabunde T, Sträter N, Fröhlich R, Witzel H, Krebs B (1996) Mechanism of Fe (III)–Zn (II) purple acid phosphatase based on crystal structures. J Mol Biol 259(4):737–748CrossRefGoogle Scholar
  43. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (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 Physiol 155(2):974–987CrossRefGoogle Scholar
  44. Kuang R, Chan K-H, Yeung E, Lim BL (2009) Molecular and biochemical characterization of AtPAP15, a purple acid phosphatase with phytase activity, in Arabidopsis. Plant physiol 151(1):199–209CrossRefGoogle Scholar
  45. Lee E-J, Iai H, Sano H, Koizumi N (2005) Sugar responsible and tissue specific expression of a gene encoding AtCIPK14, an Arabidopsis CBL-interacting protein kinase. Biosci Biotechnol Biochem 69(1):242–245CrossRefGoogle Scholar
  46. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147(2):732–746CrossRefGoogle Scholar
  47. Lin WD, Liao YY, Yang TJ, Pan CY, Buckhout TJ, Schmidt W (2011) Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant physiol 155(3):1383–1402CrossRefGoogle Scholar
  48. Lin J, Huang X, Li Q, Cao Y, Bao Y, Meng X, Li Y, Fu C, Hou B (2016) UDP-glycosyltransferase 72B1 catalyzes the glucose conjugation of monolignols and is essential for the normal cell wall lignification in Arabidopsis thaliana. Plant J 88(1):26–42CrossRefGoogle Scholar
  49. Liu J, Vance CP (2014) Crucial roles of sucrose and microRNA399 in systemic signaling of P deficiency. Plant Signal Behav 5(12):1556–1560CrossRefGoogle Scholar
  50. Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116(1):91–99CrossRefGoogle Scholar
  51. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López- Millán AF, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55(4):294–388CrossRefGoogle Scholar
  52. Mahmood T, Yasmin T, Haque MI, Naqvi SMS (2013) Characterization of a rice germin-like protein gene promoter. Genet Mol Res 12(1):360–369CrossRefGoogle Scholar
  53. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22(4):1104–1117CrossRefGoogle Scholar
  54. Maurino VG, Grube E, Zielinski J, Schild A, Fischer K, Flugge UI (2006) Identification and expression analysis of twelve members of the nucleobase-ascorbate transporter (NAT) gene family in Arabidopsis thaliana. Plant Cell Physiol 47(10):1381–1393CrossRefGoogle Scholar
  55. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y, Wininger S, Resnick N, Cohen M, Kapulnik Y, Koltai H (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160(3):1329–1341CrossRefGoogle Scholar
  56. Meyer M, Huttenlocher F, Cedzich A, Procopio S, Stroeder J, Pau-Roblot C, Lequart-Pillon M, Pelloux J, Stintzi A, Schaller A (2016) The subtilisin-like protease SBT3 contributes to insect resistance in tomato. J Exp Bot 67(14):4325–4338CrossRefGoogle Scholar
  57. Milne RJ, Perroux JM, Rae AL, Reinders A, Ward JM, Offler CE, Patrick JW, Grof CP (2017) Sucrose transporter localization and function in phloem unloading in developing stems. Plant Physiol 173(2):1330–1341CrossRefGoogle Scholar
  58. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102(33):11934–11939CrossRefGoogle Scholar
  59. Morant AV, Bjarnholt N, Kragh ME, Kjaergaard CH, Jorgensen K, Paquette SM, Piotrowski M, Imberty A, Olsen CE, Moller BL, Bak S (2008) The beta-glucosidases responsible for bioactivation of hydroxynitrile glucosides in Lotus japonicus. Plant Physiol 147(3):1072–1091CrossRefGoogle Scholar
  60. Moriyama Y, Hiasa M, Matsumoto T, Omote H (2008) Multidrug and toxic compound extrusion (MATE)-type proteins as anchor transporters for the excretion of metabolic waste products and xenobiotics. Xenobiotica 38(7–8):1107–1118CrossRefGoogle Scholar
  61. Nolte KD, Koch KE (1993) Companion-cell specific localization of sucrose synthase in zones of phloem loading and unloading. Plant Physiol 101:899–905CrossRefGoogle Scholar
  62. Notaguchi M, Okamoto S (2015) Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6:161CrossRefGoogle Scholar
  63. Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y (2017) Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat plants 3(4):17029CrossRefGoogle Scholar
  64. Okamoto S, Suzuki T, Kawaguchi M, Higashiyama T, Matsubayashi Y (2015) A comprehensive strategy for identifying long-distance mobile peptides in xylem sap. Plant J 84(3):611–620CrossRefGoogle Scholar
  65. Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17(11):2899–2910CrossRefGoogle Scholar
  66. Pizzio GA, Paez-Valencia J, Khadilkar AS, Regmi K, Patron-Soberano A, Zhang S, Sanchez-Lares J, Furstenau T, Li J, Sanchez-Gomez C, Valencia-Mayoral P, Yadav UP, Ayre BG, Gaxiola RA (2015) Arabidopsis type I proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning. Plant Physiol 167(4):1541–1553CrossRefGoogle Scholar
  67. Pommerrenig B, Barth I, Niedermeier M, Kopp S, Schmid J, Dwyer RA, McNair RJ, Klebl F, Sauer N (2006) Common plantain. A collection of expressed sequence tags from vascular tissue and a simple and efficient transformation method. Plant Physiol 142(4):1427–1441CrossRefGoogle Scholar
  68. Pommerrenig B, Papini-Terzi FS, Sauer N (2007) Differential regulation of sorbitol and sucrose loading into the phloem of Plantago major in response to salt stress. Plant Physiol 144(2):1029–1038CrossRefGoogle Scholar
  69. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50(1):665–693CrossRefGoogle Scholar
  70. Ranocha P, Denance N, Vanholme R, Freydier A, Martinez Y, Hoffmann L, Kohler L, Pouzet C, Renou JP, Sundberg B, Boerjan W, Goffner D (2010) Walls are thin 1 (WAT1). an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J 63(3):469–483CrossRefGoogle Scholar
  71. Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544CrossRefGoogle Scholar
  72. Roldan M, Dinh P, Leung S, McManus MT (2013) Ethylene and the responses of plants to phosphate deficiency. AoB Plants 5:plt013CrossRefGoogle Scholar
  73. Rouached H, Secco D, Arpat B, Poirier Y (2011) 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 11:19CrossRefGoogle Scholar
  74. Sibout R, Eudes A, Pollet B, Goujon T, Mila I, Granier F, Seguin A, Lapierre C, Jouanin L (2003) Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis. Isolation and characterization of the corresponding mutants. Plant Physiol 132(2):848–860CrossRefGoogle Scholar
  75. Song L, Liu D (2015) Ethylene and plant responses to phosphate deficiency. Front Plant Sci 6:796Google Scholar
  76. Spector AA, Yorek MA (1985) Membrane lipid composition and cellular function. J Lipid Res 26(9):1015–1035Google Scholar
  77. Stenzel I, Otto M, Delker C, Kirmse N, Schmidt D, Miersch O, Hause B, Wasternack C (2012) ALLENE OXIDE CYCLASE (AOC) gene family members of Arabidopsis thaliana: tissue- and organ-specific promoter activities and in vivo heteromerization. J Exp Bot 63(17):6125–6138CrossRefGoogle Scholar
  78. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y (2014) Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346(6207):343–346CrossRefGoogle Scholar
  79. Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221CrossRefGoogle Scholar
  80. Usuda H (1995) Phosphate deficiency in maize. V. Mobilization of nitrogen and phosphorus within shoots of young plants and its relationship to senescence. Plant Cell Physiol 36(6):1041–1049CrossRefGoogle Scholar
  81. Van de Poel B, Van Der Straeten D (2014) 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene. Front Plant Sci 5:640Google Scholar
  82. Vance CP, Uhde-Stone C, Allan DL (2002) Phosphorus acquisition and use critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447CrossRefGoogle Scholar
  83. Wang Q, Kuo L, Sjölund R, Shih M-C (1997) Immunolocalization of glyceraldehyde-3-phosphate dehydrogenase in Arabidopsis thaliana. Protoplasma 198(3):155–162CrossRefGoogle Scholar
  84. Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135(1):400–411CrossRefGoogle Scholar
  85. Weise A, Lalonde S, Kuhn C, Frommer WB, Ward JM (2008) Introns control expression of sucrose transporter LeSUT1 in trichomes, companion cells and in guard cells. Plant Mol Biol 68(3):251–262CrossRefGoogle Scholar
  86. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132(3):1260–1271CrossRefGoogle Scholar
  87. Wu H, Li L, Du J, Yuan Y, Cheng X, Ling HQ (2005) Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana. Plant Cell Physiol 46(9):1505–1514CrossRefGoogle Scholar
  88. Xu Q, Chen S, Ren Y, Chen S, Liesche J (2018) Regulation of sucrose transporters and phloem loading in response to environmental cues. Plant Physiol 176(1):930–945CrossRefGoogle Scholar
  89. Yang SY, Huang TK, Kuo HF, Chiou TJ (2017) Role of vacuoles in phosphorus storage and remobilization. J Exp Bot 68(12):3045–3055CrossRefGoogle Scholar
  90. Zhang C, Yu X, Ayre BG, Turgeon R (2012) The origin and composition of cucurbit “phloem” exudate. Plant Physiol 158(4):1873–1882CrossRefGoogle Scholar
  91. Zhang Z, Liao H, Lucas WJ (2014) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol 56(3):192–220CrossRefGoogle Scholar
  92. Zhang Z, Zheng Y, Ham BK, Chen J, Yoshida A, Kochian LV, Fei Z, Lucas WJ (2016) Vascular-mediated signalling involved in early phosphate stress response in plants. Nat Plants 2:16033CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of AgronomyPurdue UniversityWest LafayetteUSA
  2. 2.Biost Technology Co., LtdBeijingChina
  3. 3.Department of Soil and Environmental Sciences, University College of AgricultureUniversity of SargodhaSargodhaPakistan
  4. 4.The Institute of SericultureZhejiang Academy of Agricultural SciencesHangzhouChina
  5. 5.Purdue Center for Plant BiologyPurdue UniversityWest LafayetteUSA

Personalised recommendations