Tissue-specific transcriptomic profiling of Plantago major provides insights for the involvement of vasculature in phosphate deficiency responses
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 deficiencyAbbreviations
- 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
References
- Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8CrossRefGoogle Scholar
- 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
- 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
- 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
- Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4(3):377–394CrossRefGoogle Scholar
- 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
- 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
- Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206CrossRefGoogle Scholar
- Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743CrossRefGoogle Scholar
- 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
- Crafts AS (1932) Phloem anatomy, exudation, and transport of organic nutrients in cucurbits. Plant Physiol 7(2):i4CrossRefGoogle Scholar
- 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
- 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
- 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
- Esau K (1973) Comparative structure of companion cells and phloem parenchyma cells in Mimosa pudica L. Ann Bot 37(3):625–632CrossRefGoogle Scholar
- 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
- 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
- Fisher DB, Frame JM (1984) A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161:385–393CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59(1):93–109CrossRefGoogle Scholar
- 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
- 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
- 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
- Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Biol 47(1):431–444CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- King RW, Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Notaguchi M, Okamoto S (2015) Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6:161CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50(1):665–693CrossRefGoogle Scholar
- 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
- 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
- Roldan M, Dinh P, Leung S, McManus MT (2013) Ethylene and the responses of plants to phosphate deficiency. AoB Plants 5:plt013CrossRefGoogle Scholar
- 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
- 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
- Song L, Liu D (2015) Ethylene and plant responses to phosphate deficiency. Front Plant Sci 6:796Google Scholar
- Spector AA, Yorek MA (1985) Membrane lipid composition and cellular function. J Lipid Res 26(9):1015–1035Google Scholar
- 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
- 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
- Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Zhang C, Yu X, Ayre BG, Turgeon R (2012) The origin and composition of cucurbit “phloem” exudate. Plant Physiol 158(4):1873–1882CrossRefGoogle Scholar
- 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
- 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