Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Influence of cucumber mosaic virus infection on the mRNA population present in the phloem translocation stream of pumpkin plants

Roberto Ruiz-Medrano A C , Jesús Hinojosa Moya A , Beatriz Xoconostle-Cázares A and William J. Lucas B
+ Author Affiliations
- Author Affiliations

A Departamento de Biotecnología y Bioingeniería, CINVESTAV IPN. Ave. IPN 2508, Zacatenco 07360, México DF, México.

B Section of Plant Biology, College of Biological Sciences, University of California, One Shields Ave, Davis, CA 95616, USA.

C Corresponding author. Email: rmedrano@cinvestav.mx

D This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.

Functional Plant Biology 34(4) 292-301 https://doi.org/10.1071/FP06300
Submitted: 15 November 2006  Accepted: 23 January 2007   Published: 19 April 2007

Abstract

The effect of cucumber mosaic virus (CMV) infection on the phloem sap mRNA population was investigated in pumpkin Cucurbita maxima Duch. cv. Big Max, through analysis of a suppressive subtractive hybridisation (SSH) library. Analysis of the infected phloem library identified 91 highly diverse mRNA species, including enzymes involved in general metabolism, transcription factors and signalling agents. Our analysis indicated that, quantitatively, the effect of CMV infection on the composition of the phloem sap transcriptome was minor in nature. Virtual northern analysis was used to confirm the specific upregulation of these transcripts in the phloem of CMV-infected plants. In silico northern analysis also confirmed that none of the transcripts identified in the SSH library was contained in the population of mRNA species present in the phloem sap of healthy plants. Induction levels ranged from low to high and in situ hybridisation studies showed that transcripts displayed a range of accumulation patterns. Collectively, our findings suggest that plants have evolved a highly robust mechanism for the exchange of information macromolecules between the companion cell (CC) and the sieve tube system. Production of viral movement protein (MP) in the CC is not sufficient for the indiscriminate transport of mRNA into the sieve element. Our findings are discussed in the context of symptom development and likely strong selection pressure, on the viral genome, to encode for a MP that does not adversely interfere with the phloem long-distance trafficking system.


Acknowledgements

We thank Robert L. Gilbertson, Department of Plant Pathology, University of California, Davis, for providing the severe Brazilian strain of CMV. This work was supported by CONACyT-México grants 39960 (to RR-M.) and 39961 (to BX-C.) and a University of California-MEXUS grant (to RR-M. and WJL). JH-M. was supported by a doctoral fellowship from CONACyT-México. This manuscript is dedicated to the memory of our colleague and friend, Vincent Ray Franceschi.


References


Aoki K, Suzui N, Fujimaki S, Dohmae N, Yonekura-Sakakibara K, Fujiwara T, Hayashi H, Yamaya T, Sakakibara H (2005) Destination-selective long-distance movement of phloem proteins. Plant Cell 17, 1801–1814.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Morelli G (2001) The Arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiology 126, 643–655.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ (1997) Phloem sap proteins of Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proceedings of the National Academy of Sciences USA 94, 14150–14155.
Crossref | GoogleScholarGoogle Scholar | open url image1

Beveridge CA (2006) Axillary bud outgrowth: sending a message. Current Opinion in Plant Biology 9, 35–40.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Beyenbach J, Weber C, Kleinig H (1974) Sieve-tube proteins from Cucurbita maxima. Planta 119, 113–124.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carrington JC, Kasschau KD, Mahajan SK, Schaad MC (1996) Cell-to-cell and long-distance transport of viruses in plants. The Plant Cell 8, 1669–1681.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. Journal of Biological Chemistry 278, 23747–23752.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Mogadam F , et al. (1996) Suppression subtractive hybridisation: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences USA 93, 6025–6030.
Crossref |
open url image1

Doering-Saad C, Newbury HJ, Couldridge CE, Bale JS, Pritchard J (2006) A phloem-enriched cDNA library from Ricinus: insights into phloem function. Journal of Experimental Botany 57, 3183–3193.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O (2004) Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. The Plant Cell 16, 1235–1250.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Durrant WE, Dong X (2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185–209.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Giavalisco P, Kapitza A, Kolasa A, Buhtz A, Kehr J (2006) Towards the proteome of Brassica napus phloem sap. Proteomics 6, 896–909.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gilbertson RL, Lucas WJ (1996) How do viruses traffic on the ‘vascular highway’? Trends in Plant Science 1, 250–251.
Crossref | GoogleScholarGoogle Scholar | open url image1

Haywood V, Yu TS, Huang NT, Lucas WJ (2005) Phloem-long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. The Plant Journal 42, 49–68.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Huang T, Bohlenius H, Eriksson S, Parcy F, Nilsson O (2005) The mRNA of the Arabidopsis gene FT moves from leaf to shoot apex and induces flowering. Science 309, 1694–1696.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293, 287–289.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kim JY, Rim Y, Wang L, Jackson D (2005) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes & Development 19, 788–793.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275, 1298–1300.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annual Review of Plant Biology 55, 341–372.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Analytical Biochemistry 163, 16–20.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lough T, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annual Review of Plant Biology 57, 203–232.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mellor J (2006) It takes a PHD to read the histone code. Cell 126, 22–24.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ohashi-Ito K, Fukuda H (2003) HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant & Cell Physiology 44, 1350–1358.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruiz-Medrano R, Xoconostle-Cázares B, Lucas WJ (1999) Phloem long-distance trasnport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126, 4405–4419.
PubMed |
open url image1

Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signalling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299, 109–112.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant, Cell & Environment 26, 125–149.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wang Z, Dai L, Jiang Z, Peng W, Zhang L, Wang G, Xie D (2005) GmCOI1, a soybean F-box protein gene, shows ability to mediate jasmonate-regulated plant defense and fertility in Arabidopsis. Molecular Plant–Microbe Interactions 18, 1285–1295.
PubMed |
open url image1

Xoconostle-Cázares B, Xiang Y, Ruiz-Medrano R, Wang H-L, Monzer J, Yoo B-C, McFarland KC, Franceschi VR, Lucas WJ (1999) Plant paralog to viral movement protein potentiates transport of mRNA into the phloem. Science 283, 94–98.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xoconostle-Cazares B, Ruiz-Medrano R, Lucas WJ (2000) Proteolytic processing of CmPP36, a protein from the cytochrome b(5) reductase family, is required for entry into the phloem translocation pathway. The Plant Journal 24, 735–747.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zeevaart JA (1962) Physiology of flowering. Science 137, 723–731.
Crossref | GoogleScholarGoogle Scholar | open url image1