Plasmodesmata: the battleground against intruders
2011; Elsevier BV; Volume: 16; Issue: 4 Linguagem: Inglês
10.1016/j.tplants.2011.01.004
ISSN1878-4372
Autores Tópico(s)Plant Virus Research Studies
ResumoPlasmodesmata are intercellular channels that establish a symplastic communication pathway between neighboring cells in plants. Owing to this role, opportunistic microbial pathogens have evolved to exploit plasmodesmata as gateways to spread infection from cell to cell within the plant. However, although these pathogens have acquired the capacity to breach the plasmodesmal trafficking pathway, plants are unlikely to relinquish control over a structure essential for their survival so easily. In this review, we examine evidence that suggests plasmodesmata play an active role in plant immunity against viral, fungal and bacterial pathogens. We discuss how these pathogens differ in their lifestyles and infection modes, and present the defense strategies that plants have adopted to prevent the intercellular spread of an infection. Plasmodesmata are intercellular channels that establish a symplastic communication pathway between neighboring cells in plants. Owing to this role, opportunistic microbial pathogens have evolved to exploit plasmodesmata as gateways to spread infection from cell to cell within the plant. However, although these pathogens have acquired the capacity to breach the plasmodesmal trafficking pathway, plants are unlikely to relinquish control over a structure essential for their survival so easily. In this review, we examine evidence that suggests plasmodesmata play an active role in plant immunity against viral, fungal and bacterial pathogens. We discuss how these pathogens differ in their lifestyles and infection modes, and present the defense strategies that plants have adopted to prevent the intercellular spread of an infection. Eduard Tangl first recognized the plasmodesma some hundred years ago as a fundamental structure that allows plants to form advanced multicellular organisms [1Gunning B.E.S. Introduction to plasmodesmata.in: Gunning B.E.S. Robards A.W. Intercellular Communication in Plants: Studies on Plasmodesmata. Springer-Verlag, 1976: 1-13Crossref Google Scholar]. Molecular analyses now support the idea that the development of plasmodesmata is one of the most crucial events in the evolution of higher plants [2Karol K.G. et al.The closest living relatives of land plants.Science. 2001; 294: 2351-2353Crossref PubMed Scopus (463) Google Scholar, 3Graham L.E. et al.The origin of plants: body plan changes contributing to a major evolutionary radiation.Proc. Natl. Acad. Sci. U.S.A. 2000; 97: 4535-4540Crossref PubMed Scopus (278) Google Scholar]. Once thought to be simple 'holes' in plant cell walls that mediate only the passive diffusion of small molecules [4Maule A.J. Plasmodesmata: structure, function and biogenesis.Curr. Opin. Plant Biol. 2008; 11: 680-686Crossref PubMed Scopus (139) Google Scholar, 5Kim I. Zambryski P.C. Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis.Curr. Opin. Plant Biol. 2005; 8: 593-599Crossref PubMed Scopus (86) Google Scholar, 6Lucas W.J. Lee J.Y. Plasmodesmata as a supracellular control network in plants.Nat. Rev. Mol. Cell Biol. 2004; 5: 712-726Crossref PubMed Scopus (299) Google Scholar, 7Lucas W.J. et al.Plasmodesmata – bridging the gap between neighboring plant cells.Trends Cell Biol. 2009; 19: 495-503Abstract Full Text Full Text PDF PubMed Scopus (208) Google Scholar, 8Heinlein M. Epel B.L. Macromolecular transport and signaling through plasmodesmata.Int. Rev. Cytol. 2004; 235: 93-164Crossref PubMed Scopus (126) Google Scholar, 9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 10Ding B. et al.Symplasmic protein and RNA traffic: regulatory points and regulatory factors.Curr. Opin. Plant Biol. 2003; 6: 596-602Crossref PubMed Scopus (73) Google Scholar, 11Cilia M.L. Jackson D. Plasmodesmata form and function.Curr. Opin. Plant Biol. 2004; 16: 500-506Crossref Scopus (71) Google Scholar], studies over the past two decades have led to a complete change in scientific understanding of this essential structure. Plasmodesmata are now known to be structurally complex, with the capacity to dilate and facilitate the cell-to-cell transport of macromolecules, such as proteins, RNAs and protein–RNA complexes. Furthermore, they are also functionally dynamic channels, undergoing modifications in permeability, or changes in positional frequency along the cell wall, depending on the needs of the plant [12Ehlers K. Kollmann R. Primary and secondary plasmodesmata: structure, origin, and functioning.Protoplasma. 2001; 216: 1-30Crossref PubMed Scopus (157) Google Scholar, 13Robards A.W. Lucas W.J. Plasmodesmata.Annu. Rev. Plant Physiol. Plant Mol. Biol. 1990; 41: 369-419Crossref Scopus (311) Google Scholar, 14Lee J.Y. et al.Plasmodesmata and non-cell-autonomous signaling in plants.in: Murphy A.S. The Plant Plasma Membrane. 1st edn. Springer, 2010: 87-108Google Scholar]. These characteristics allow plasmodesmata to establish domains of symplastically connected cells, so-called 'symplastic domains,' giving higher plants a means to produce different cell types, tissues and organs; they can also form cellular gateways to the vascular system, enabling plants to coordinate cellular responses at the whole-organism level [9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 15Lough T.J. Lucas W.J. Integrative plant biology: role of phloem long-distance macromolecular trafficking.Annu. Rev. Plant Biol. 2006; 57: 203-232Crossref PubMed Scopus (417) Google Scholar, 16Turgeon R. Wolf S. Phloem transport: cellular pathways and molecular trafficking.Annu. Rev. Plant Biol. 2009; 60: 207-221Crossref PubMed Scopus (357) Google Scholar]. Plasmodesmata form long, cylindrical plasma membrane (PM)-lined bridges between neighboring cells across their cell walls (Figure 1a) . The cytoplasmic sleeve delimited by the PM within plasmodesmata is occupied by the appressed endoplasmic reticulum (ER) strand and proteinaceous components, which add intricate structural and mechanistic elements to each channel. It is presumed that soluble molecules are transported passively through the cytoplasmic sleeves, which are subdivided into microchannels of 3–4 nm in diameter within the space between the ER and PM [4Maule A.J. Plasmodesmata: structure, function and biogenesis.Curr. Opin. Plant Biol. 2008; 11: 680-686Crossref PubMed Scopus (139) Google Scholar, 9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 13Robards A.W. Lucas W.J. Plasmodesmata.Annu. Rev. Plant Physiol. Plant Mol. Biol. 1990; 41: 369-419Crossref Scopus (311) Google Scholar]. Plasmodesmata can also actively facilitate intercellular trafficking of a special class of endogenous proteins, called non-cell autonomous proteins (NCAPs), and various types of RNA [6Lucas W.J. Lee J.Y. Plasmodesmata as a supracellular control network in plants.Nat. Rev. Mol. Cell Biol. 2004; 5: 712-726Crossref PubMed Scopus (299) Google Scholar, 9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 17Haywood V. et al.Plasmodesmata: pathways for protein and ribonucleoprotein signaling.Plant Cell. 2002; 14: S303-S325Crossref PubMed Scopus (188) Google Scholar]. Many NCAPs, particularly those that act as transcription factors, have been implicated in developmental processes, such as cell-type specification and differentiation [6Lucas W.J. Lee J.Y. Plasmodesmata as a supracellular control network in plants.Nat. Rev. Mol. Cell Biol. 2004; 5: 712-726Crossref PubMed Scopus (299) Google Scholar, 11Cilia M.L. Jackson D. Plasmodesmata form and function.Curr. Opin. Plant Biol. 2004; 16: 500-506Crossref Scopus (71) Google Scholar, 17Haywood V. et al.Plasmodesmata: pathways for protein and ribonucleoprotein signaling.Plant Cell. 2002; 14: S303-S325Crossref PubMed Scopus (188) Google Scholar, 18Gallagher K.L. Benfey P.N. Not just another hole in the wall: understanding intercellular protein trafficking.Genes Dev. 2005; 19: 189-195Crossref PubMed Scopus (74) Google Scholar]. Callose (Box 1), a β-1,3 glucan polymer, can be considered a regulatory component of plasmodesmata (Figure 1a) because its deposition at the plasmodesmal orifice can physically constrict the dimension of the opening, reducing the size exclusion limit (SEL), or even seal it completely, blocking plasmodesmal trafficking [19Radford J.E. et al.Callose deposition at plasmodesmata.Protoplasma. 1998; 201: 30-37Crossref Scopus (131) Google Scholar].Box 1CalloseCallose, a β-1,3 glucan cell wall polymer, is one of the prominent, non-proteinaceous components associated with plasmodesmata. It is reversibly deposited within the cell wall surrounding the neck region of the plasmodesma (Figure I) in response to various stress conditions [9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 19Radford J.E. et al.Callose deposition at plasmodesmata.Protoplasma. 1998; 201: 30-37Crossref Scopus (131) Google Scholar]. Callose deposition is controlled by callose synthases and β-1,3 glucanases [75Brownfield L. et al.Biochemical and molecular properties of biosynthetic enzymes for (1,3)-b-glucans.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 283-326Crossref Scopus (14) Google Scholar]. Arabidopsis (Arabidopsis thaliana) encodes 12 members of the glucan synthase-like enzyme family that are predicted to function as callose synthases [76Dong X. et al.Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection.Planta. 2008; 229: 87-98Crossref PubMed Scopus (105) Google Scholar] and over 40 β-1,3 glucanases [75Brownfield L. et al.Biochemical and molecular properties of biosynthetic enzymes for (1,3)-b-glucans.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 283-326Crossref Scopus (14) Google Scholar]. Reversible control over plasmodesmal permeability would be best achieved by positioning both callose synthase and hydrolase at the plasmodesma. Indeed, a β-1,3 glucanase has been shown to be targeted to plasmodesmata [68Levy A. et al.A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis.Plant J. 2007; 49: 669-682Crossref PubMed Scopus (254) Google Scholar] and one of the callose synthases has been implicated in controlling plasmodesmal trafficking [77Guseman J.M. et al.Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8).Development. 2010; 137: 1731-1741Crossref PubMed Scopus (169) Google Scholar].Figure ICallose deposition at plasmodesmata. (a) A false-colored confocal image of aniline blue fluorescence shows plasmodesmata as punctate signals (arrowheads) at the epidermal cell junctions of Arabidopsis leaf tissue. Scale bar = 20 μm. (b) Immunogold detection of callose (arrowheads) at a plasmodesma (PD). Scale bar = 200 nm. Abbreviations: CW, cell wall; Cyt 1, cell 1 cytoplasm; Cyt 2, cell 2 cytoplasm; ML, middle lamella. Reproduced, with permission, from J-Y. Lee.View Large Image Figure ViewerDownload (PPT)Callose does not constitute a main component of cell walls in higher plants but is found during normal development in specialized cell types, including reproductive tissues, and occurs transiently in walls undergoing remodeling or cell division [75Brownfield L. et al.Biochemical and molecular properties of biosynthetic enzymes for (1,3)-b-glucans.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 283-326Crossref Scopus (14) Google Scholar, 78Hong Z. et al.A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate.Plant Cell. 2001; 13: 769-779Crossref PubMed Scopus (147) Google Scholar]. During the formation of sieve plate pores in phloem cells, massive callose accumulation at the cell wall surrounding the plasmodesma precedes disintegration of the latter, eventually leaving open pores following callose removal [79Esau K. Thorsch J. Sieve plate pores and plasmodesmata, the communication channels of the symplast – ultrastructural aspects and developmental relations.Am. J. Bot. 1985; 72: 1641-1653Crossref Google Scholar] (Figure II). Callose is also produced in response to abiotic and biotic stresses at the sites of mechanical wounding or pathogen penetration, providing a scaffold for repairing the damaged cell membrane and wall, or reinforcing the wall itself. Upon fungal pathogen attack, plants form a local cell wall apposition, called a papilla, which is rich in callose [80Voigt C.A. Somerville S.C. Callose in biotic stress (pathogenesis) biology, biochemistry and molecular biology of callose in plant defence: callose deposition and turnover in plant–pathogen interactions.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 525-562Crossref Scopus (17) Google Scholar]. The function of this callose in plant–microbe interactions is not yet fully understood.Figure IITransient callose accumulation during sieve plate pore formation. A simplified model depicting development of sieve plates [79Esau K. Thorsch J. Sieve plate pores and plasmodesmata, the communication channels of the symplast – ultrastructural aspects and developmental relations.Am. J. Bot. 1985; 72: 1641-1653Crossref Google Scholar]. (a) Plasmodesmata (PD) at the future pore sites. (b) A massive callose deposition occurs at the plasmodesmata, which is followed by (c) degeneration of appressed ER and widening of the plasmodesmal cytoplasmic space. Callose plugs are degraded, and open pores with residual callose are formed in the mature sieve plate (d).View Large Image Figure ViewerDownload (PPT)The regulation of callose synthesis has been closely linked to the SA signaling pathway, a key defense pathway with a crucial role in plant resistance to not only bacterial, but also viral and fungal pathogens [81Vlot A.C. et al.Salicylic acid, a multifaceted hormone to combat disease.Annu. Rev. Phytopathol. 2009; 47: 177-206Crossref PubMed Scopus (1757) Google Scholar]. Several Arabidopsis callose synthase genes are induced by exogenous SA treatment, suggesting SA-dependent and -independent modes of callose synthesis [76Dong X. et al.Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection.Planta. 2008; 229: 87-98Crossref PubMed Scopus (105) Google Scholar]. Several HR-cell death mutants that accumulate a high level of SA have also led to constitutive defense responses and upregulated callose deposition [82Lu H. et al.ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response.Plant Cell. 2003; 15: 2408-2420Crossref PubMed Scopus (162) Google Scholar, 83Consonni C. et al.Conserved requirement for a plant host cell protein in powdery mildew pathogenesis.Nat. Genet. 2006; 38: 716-720Crossref PubMed Scopus (399) Google Scholar]. Conversely, suppression of SA accumulation by introducing a mutation that impairs SA biosynthesis has been correlated with a reduced callose level [55DebRoy S. et al.A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants.Proc. Natl. Acad. Sci. U.S.A. 2004; 101: 9927-9932Crossref PubMed Scopus (284) Google Scholar]. Callose, a β-1,3 glucan cell wall polymer, is one of the prominent, non-proteinaceous components associated with plasmodesmata. It is reversibly deposited within the cell wall surrounding the neck region of the plasmodesma (Figure I) in response to various stress conditions [9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 19Radford J.E. et al.Callose deposition at plasmodesmata.Protoplasma. 1998; 201: 30-37Crossref Scopus (131) Google Scholar]. Callose deposition is controlled by callose synthases and β-1,3 glucanases [75Brownfield L. et al.Biochemical and molecular properties of biosynthetic enzymes for (1,3)-b-glucans.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 283-326Crossref Scopus (14) Google Scholar]. Arabidopsis (Arabidopsis thaliana) encodes 12 members of the glucan synthase-like enzyme family that are predicted to function as callose synthases [76Dong X. et al.Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection.Planta. 2008; 229: 87-98Crossref PubMed Scopus (105) Google Scholar] and over 40 β-1,3 glucanases [75Brownfield L. et al.Biochemical and molecular properties of biosynthetic enzymes for (1,3)-b-glucans.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 283-326Crossref Scopus (14) Google Scholar]. Reversible control over plasmodesmal permeability would be best achieved by positioning both callose synthase and hydrolase at the plasmodesma. Indeed, a β-1,3 glucanase has been shown to be targeted to plasmodesmata [68Levy A. et al.A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis.Plant J. 2007; 49: 669-682Crossref PubMed Scopus (254) Google Scholar] and one of the callose synthases has been implicated in controlling plasmodesmal trafficking [77Guseman J.M. et al.Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8).Development. 2010; 137: 1731-1741Crossref PubMed Scopus (169) Google Scholar]. Callose does not constitute a main component of cell walls in higher plants but is found during normal development in specialized cell types, including reproductive tissues, and occurs transiently in walls undergoing remodeling or cell division [75Brownfield L. et al.Biochemical and molecular properties of biosynthetic enzymes for (1,3)-b-glucans.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 283-326Crossref Scopus (14) Google Scholar, 78Hong Z. et al.A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate.Plant Cell. 2001; 13: 769-779Crossref PubMed Scopus (147) Google Scholar]. During the formation of sieve plate pores in phloem cells, massive callose accumulation at the cell wall surrounding the plasmodesma precedes disintegration of the latter, eventually leaving open pores following callose removal [79Esau K. Thorsch J. Sieve plate pores and plasmodesmata, the communication channels of the symplast – ultrastructural aspects and developmental relations.Am. J. Bot. 1985; 72: 1641-1653Crossref Google Scholar] (Figure II). Callose is also produced in response to abiotic and biotic stresses at the sites of mechanical wounding or pathogen penetration, providing a scaffold for repairing the damaged cell membrane and wall, or reinforcing the wall itself. Upon fungal pathogen attack, plants form a local cell wall apposition, called a papilla, which is rich in callose [80Voigt C.A. Somerville S.C. Callose in biotic stress (pathogenesis) biology, biochemistry and molecular biology of callose in plant defence: callose deposition and turnover in plant–pathogen interactions.in: Bacic A. Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides. Elsevier, 2009: 525-562Crossref Scopus (17) Google Scholar]. The function of this callose in plant–microbe interactions is not yet fully understood. The regulation of callose synthesis has been closely linked to the SA signaling pathway, a key defense pathway with a crucial role in plant resistance to not only bacterial, but also viral and fungal pathogens [81Vlot A.C. et al.Salicylic acid, a multifaceted hormone to combat disease.Annu. Rev. Phytopathol. 2009; 47: 177-206Crossref PubMed Scopus (1757) Google Scholar]. Several Arabidopsis callose synthase genes are induced by exogenous SA treatment, suggesting SA-dependent and -independent modes of callose synthesis [76Dong X. et al.Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection.Planta. 2008; 229: 87-98Crossref PubMed Scopus (105) Google Scholar]. Several HR-cell death mutants that accumulate a high level of SA have also led to constitutive defense responses and upregulated callose deposition [82Lu H. et al.ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response.Plant Cell. 2003; 15: 2408-2420Crossref PubMed Scopus (162) Google Scholar, 83Consonni C. et al.Conserved requirement for a plant host cell protein in powdery mildew pathogenesis.Nat. Genet. 2006; 38: 716-720Crossref PubMed Scopus (399) Google Scholar]. Conversely, suppression of SA accumulation by introducing a mutation that impairs SA biosynthesis has been correlated with a reduced callose level [55DebRoy S. et al.A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants.Proc. Natl. Acad. Sci. U.S.A. 2004; 101: 9927-9932Crossref PubMed Scopus (284) Google Scholar]. The direct, symplastic connections provided by plasmodesmata confer numerous biological advantages to plants for coordinating physiological and developmental processes. However, some biotrophic microbial pathogens see plasmodesmata as an opportunity for easy travel and hijack the symplastic passageways for infection. This situation has been well documented for plant viruses, which are tiny parasites on a nanometer scale [8Heinlein M. Epel B.L. Macromolecular transport and signaling through plasmodesmata.Int. Rev. Cytol. 2004; 235: 93-164Crossref PubMed Scopus (126) Google Scholar, 9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 10Ding B. et al.Symplasmic protein and RNA traffic: regulatory points and regulatory factors.Curr. Opin. Plant Biol. 2003; 6: 596-602Crossref PubMed Scopus (73) Google Scholar]. Surprisingly, pathogens larger than viruses, such as hemibiotrophic fungi, have also been found to spread by growing into uninfected cells through plasmodesmata [20Kankanala P. et al.Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus.Plant Cell. 2007; 19: 706-724Crossref PubMed Scopus (424) Google Scholar]. These cases illustrate the fact that the pathogens might have acquired the capacity to recognize and/or remodel plasmodesmata for their benefit, while keeping the plant cell membrane intact during their invasion processes to prevent elicitation of plant defense or cell death responses. In this review, we examine what is known about how plants cope with biotrophic pathogens that breach plasmodesmata for cell-to-cell infection, and which molecular players and mechanisms regulate plasmodesmata against these microbes. Although the relevant information is largely limited to viral systems, we focus here on common themes between viral, fungal and bacterial pathogens, with emphasis on how each might exploit plasmodesmata in their modes of infection. We also dissect the plant defense signaling pathways elicited by these pathogens to gain an understanding of how plasmodesmata might play a role. Given the detrimental consequences for the plant that would result from a loss of control over plasmodesmata, we propose that safeguarding and manipulating plasmodesmal structure and function might constitute a significant part of the defense mechanism in higher plants. The plant vascular system comprises the xylem, which distributes water and minerals absorbed through the roots into all tissues, and the phloem, which transports the photosynthates produced in mature leaves across the plant (Figure 1c) [15Lough T.J. Lucas W.J. Integrative plant biology: role of phloem long-distance macromolecular trafficking.Annu. Rev. Plant Biol. 2006; 57: 203-232Crossref PubMed Scopus (417) Google Scholar, 16Turgeon R. Wolf S. Phloem transport: cellular pathways and molecular trafficking.Annu. Rev. Plant Biol. 2009; 60: 207-221Crossref PubMed Scopus (357) Google Scholar]. Xylem, which is devoid of cellular membranes at maturity, constitutes the apoplastic pathway and mediates unidirectional, root-to-shoot signaling. By contrast, phloem comprises living cells and, therefore, forms the symplastic pathway, with flow direction determined on the basis of sink–source relationships. Plasmodesmata, which function as gateways to this symplastic pathway, are essential for molecular entry into, and exit from, the phloem, facilitating the distribution of nutrients and other important factors (Figure 1b). In essence, plasmodesmata enable the integration of local cell communication into long-distance signaling a capability without which higher plants could not exist [6Lucas W.J. Lee J.Y. Plasmodesmata as a supracellular control network in plants.Nat. Rev. Mol. Cell Biol. 2004; 5: 712-726Crossref PubMed Scopus (299) Google Scholar, 9Roberts A.G. Oparka K.J. Plasmodesmata and the control of symplastic transport.Plant Cell Environ. 2003; 26: 103-124Crossref Scopus (285) Google Scholar, 14Lee J.Y. et al.Plasmodesmata and non-cell-autonomous signaling in plants.in: Murphy A.S. The Plant Plasma Membrane. 1st edn. Springer, 2010: 87-108Google Scholar, 15Lough T.J. Lucas W.J. Integrative plant biology: role of phloem long-distance macromolecular trafficking.Annu. Rev. Plant Biol. 2006; 57: 203-232Crossref PubMed Scopus (417) Google Scholar]. The default biogenesis of a primary plasmodesma occurs during the formation of the cell plate in dividing daughter cells. Theoretically, all cells could remain connected in a single, plant-wide symplast. However, this is not a desirable trait; cells need highly localized signals, separate from cells in the surrounding area, to differentiate into specific types, forming the various tissues and organs of the plant. Indeed, higher plants have acquired dynamic control over the formation of symplastic domains by altering the frequency of plasmodesmata between cells and fine tuning plasmodesmal permeability at given cell junctions and developmental stages [21Rinne P.L.H. van der Schoot C. Plasmodesmata at the crossroads between development, dormancy, and defense.Can. J. Bot. 2003; 81: 1182-1197Crossref Scopus (53) Google Scholar]. Post-cytokinetic, de novo biosynthesis of secondary plasmodesmata during cell expansion helps to maintain plasmodesmal density by increasing the total number of plasmodesmata across the growing cell wall [22Faulkner C. et al.Peeking into pit fields – a new model of secondary plasmodesmata formation.Comp. Biochem. Physiol. Mol. Integr. Physiol. 2008; 150: S140-S141Crossref Google Scholar, 23Faulkner C. et al.Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation in tobacco.Plant Cell. 2008; 20: 1504-1518Crossref PubMed Scopus (106) Google Scholar]. Plasmodesmata can also undergo degeneration at selected cell–cell interfaces to isolate particular cell types, allowing them to perform a specialized cellular function. This occurs irreversibly in mature guard cells but spatiotemporally during phase changes, such as the floral transition [24Ormenese S. et al.Cytokinin application to the shoot apical meristem of Sinapis alba enhances secondary plasmodesmata formation.Planta. 2006; 224: 1481-1484Crossref PubMed Scopus (28) Google Scholar, 25Ormenese S. et al.The shoot apical meristem of Sinapis alba L. expands its central symplasmic field during the floral transition.Planta. 2002; 215: 67-78Crossref PubMed Scopus (32) Google Scholar, 26Ormenese S. et al.The frequency of plasmodesmata increases early in the whole shoot apical meristem of Sinapis alba L. during floral transition.Planta. 2000; 211: 370-375Crossref PubMed Scopus (46) Google Scholar]. Plants can modify the symplastic connectivity in response to environmental cues and challenges to bring about appropriate biochemical and physiological changes both at the local and whole-plant levels [6Lucas W.J. Lee J.Y. Plasmodesmata as a supracellular control network in plants.Nat. Rev. Mol. Cell Biol. 2004; 5: 712-726Crossref PubMed Scopus (299) Google Scholar]. For example, controlled plant cell death under incompatible microbial attack is one of the most prevailing defense responses, preventing the spread of infection by confining the pathogen locally in dead cells [27Greenberg J.T. Yao N. The role and regulation of programmed cell death in plant–pathogen interactions.Cell Microbiol. 2004; 6: 201-211Crossref PubMed Scopus (579) Google Scholar]. The role of plasmodesmata in this process has not been experimentally addressed, but it is conceivable that closure of the cellular borders would be vital to block diffusion of any toxic molecules, produced by either infected cells or microbes, into the healthy neighboring cells [21Rinne P.L.H. van der Schoot C. Plasmodesmata at the crossroads between development, dormancy, and defense.Can. J. Bot. 2003; 81: 1182-1197Crossref Scopus (53) Google Scholar, 27Greenberg J.T. Yao N. The role and regu
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