Cell interactions in plants Philip W. Becraft and Michael Freeling U n i v e r s i t y of California, Berkeley, California, USA
Plant cells interact during development through diverse mechanisms that range from genetically encoded signals to physical stresses. Pollen self-incompatibility is the best understood cell interaction in plants. Analysis of genes that appear to be involved in specific developmental signals, such as liguleless'l from maize and GLABROUS1 from Arabidopsis, will provide clues as to the nature of cell interactions in plant development. Recent data suggest that intercellular connections may be more similar in plants and animals than previously thought.
Current Opinion in Genetics and Development 1992, 2:571-575
Introduction
Experimental evidence of cell interactions
Plants are structurally simple as compared with animals and do not undergo complex morphogenetic movements. Nonetheless, plants must contend with problems of coordinating cellular growth and differentiation, cell recognition, and even cell migration. Clonal analysis shows that plant cells remmn pluripotent until relatively late in development; therefore cell interactions detem~ine the fate of most plant cells [1o,2o]. Our present knowledge of plant cell interactions is limited and mainly phenomenological. For example, cells in the meristem must interact to coordinate activity. Phyllotax3,, mitotic activity, patterns of gene expression and phase transitions -all require coordination among meristematic cells. Classic experiments where surgically bisected meristems reorganized into two complete meristems have demonstrated that meristems are functionally integrated [3]. Several genes controlling the transition to a floral meristem and the identity of floral organs have recently been isolated (reviewed in [4°']). Cell interactions must be required for the manifestation of the phenotypes these genes confer, and some indirect evidence suggests that tile floricaula gene may participate in cell communication [1°], but the way cells within a meristem communicate is still not understood.
This paper reviews work from the past year that is relevant to the subject of plant cell interactions. Emphasis is on cell interactions in higher plant development. Individ. ual topics are discussed briefly as this is a broad field. The is considerable information concerning host-pathogen interactions in plants will not be covered.
Pollen-pistil interactions The clearest examples of cell interactions in plants are those between pollen and the pistil. The pollen and stigma must recognize compatible pollinations, and then file pollen tube migrates through the transmitting tissue of the pistil to the embryo sac where fertilization occurs. This has mostly been studied in self-incompatible plants. Self-incompatibility ensures outcrossing by preventing pollination of a flower by pollen of the same genotype. In gametophytic incompatibility, pollination is blocked if the haploid pollen carries either of the two S-alleles carried by the diploid stigmatic tissue. In Nicc~ tiana alata, the S-locus encodes a glycoprotein RNase that can enter the cytoplasm of in vitro grown pollen and inhibit protein synthesis [5]. This effect was, however, seen for both compatible and incompatible allelic combinations of S-RNase and pollen thus suggesting that other factors may be involved in vivo. In sporophytic self-incompatibility systems such as that occurring in Brassica, pollen germination is inhibited if file stigma carries either of the two S-alleles carried by the diploid pollen parent, regardless of the genotype of the pollen per se (reviewed in [6]). Polymorphisms in the S-locus glycoprotein (SLG) gene strongly correlate with the pollen incompatibility phenotype. Fusion of the SLG promoter to a [B-glucuronidase (GUS) reporter gene showed that SLG was expressed, as expected, in the stigma and transmitting tract of the style and also in the tapetum, which acts as a nurse tissue for developing pollen [7"]. SLG alone does not, however, appear to confer a self-incompatibility phenotype in transgenic
Abbreviations ABP--auxin-binding protein; glbT--glabrousl; GUS~-glucuronidase; IAA--indole-3-acetic acid; Igl--ligulelessl; SLG--S-Iocus glycoprotein; SRG--S-related genes.
(~) Current Biology Ltd ISSN 0959-437X
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Pattern formation and developmental mechanisms plants [8°-]. Several S-related genes (SRG) have been identified both linked and unlinked to tile S-locus [9]. An SRG that is tightly linked to, and presumed to reside at, the S-locus was cloned and encodes a putative receptor kinase, based on predicted mnino-acid sequence [8,°]. Transcripts from this gene were detected exclusively in pistils and anthers, and analysis of several alleles showed a high degree of polymorphism. This suggests that the receptor kinase m W have a role in self-incompatibility.
Cell interactions in leaf development Recent studies have identified cell interactions invoh,ed in coordinating leaf differentiation. Maize leaves consist of the morphologically distinct blade and sheath. These join at the ligular region that consists of a tissue fringe called tile ligule and two triangnlar structures called auricles, which act as a hinge. Recessive ligulelessl (Igl) mutants lack ligules and auricles. In genetic mosaics, the wild-type Lgl allele acts autonomously although tile wildtype mesophyil can induce a rudimentary ligule in mutant epidermis directly overlaying it [10]. Furthemlore, when lgl mutant sectors interrupted the ligule, they caused the ligule on the marginal side of the sector to be displaced basipetally relative to the ligule on the other side of the sector [11-]. This suggested a model in which the mutant sectors blocked the transmission of a signal that organizes the ligular region, thus causing a delayed ligule initiation on the marginal side. Because leaf differentiation proceeds basipetally, this delay resulted in a more basal ligule position. Thus die LGI gene appears to be required for reception or transmission of this signal. In Arabidops& glabrousl (glbl) mutants lack the hairlike epidermal trichome cells on leaves, petioles, sepals and stems, and appear to have no other defect. The DNA sequence of this gene encodes a protein with a Myb DNAbinding domain [12-.]. The GLB1 promoter was fused to a GUS reporter gene and transformed into wild-type Arabidopsis. No expression was detected in trichomes; GUS staining occurred only in stipules, small appendages at the base of leaves [12-]. This suggests that GLB1 regulates the production of a diffusible factor in stipules that induces trichome fom~ation in other organs. A genetic mosaic analysis would be a more rigorous test of this hypothesis. The leaf vasculature has been implicated as having an organizational role during leaf development. Lateral veins of maize leaves are the site of action for dominant Knottedl mutations although other cells including epidermis are induced to divide [13]. Kp,ottedl was tile first plant homeobox gene identified [14-]. As such, Knottedl alters the development of veins which then appear to regulate epidermal cell divisions through cell interactions. Veins also appear central to the developmental anatomy of plants that exhibit C4-type photosynthesis. While C3 plants perform all their photosynthesis in a single cell type, C4 plants divide their photosynthetic reactions between mesophyll cells and vascular bundle sheath cells. These different photosynthetic cell types are arranged in a specialized organization called the Kranz anatomy [15]. In the blade of maize, veins are tightly packed and all mesophyll cells express C4 enzymes. In contrast, in
the sheaths and husk leaves, veins are widely spaced and mesophyll cells in close proximity to veins express C4 enzymes while at a distance dley express C3 enzymes. As such, the veins appear to produce a signal that induces C4 development. Although the nature of this signal is unclear, C4 gene expression is l)roperly compartmentalized from the outset of vascular differentiation, kal interesting new maize mutant, bundle sheath defective, has normal C4 mesophyll but the bundle sheath ceils fail to differentiate properly (JA Langdale, abstract 78, 34th Annual Maize Genetics Conference, Asilomar, California, March 1991). A lesion in the signaling mechmxism is a possible explanation for this phenotype. In tile dicotyledonous C4 Amaranthus, the C4 pattern of photosynthetic enzyme expression is not immediately expressed but becomes established after vascular differentiation [16]. Thus cells may interact somewhat differently in processes that are similar between monocots and dicots. A striking feature of leaf epidermis is the regular pattern of stomata. In Sansevieria leaves, many stomata arrest during development. The pattern of mature stomata is more regular than that of the immature stomata, suggesting that developing stomata interact with their surrounding tissue and that an epigenetic selection mechanism allows maturation ocdy of properly spaced stomata [17]. "Laser ablation of stomatal initials in similarly patterned D'adescantia leaves caused no change in stomatal pattern; however, deteru~inative events may have already occurred [18].
Signal molecules Auxins are the most studied of the classic phytohormones and are involved in many plant responses, both short- and long-range. The current challenge is to elucidate auxin receptors and signal transduction pathways (reviewed in [19] ). Auxin-binding proteins (ABPs) have been identified in the plasma membrane, endoplasmic reticulum, nucleus and cTtosol [19,20..,21.]. In tobacco protoplasts, sensitivity to auxin correlated with the amount of cross-reactivity to maize anti-ABP antibodies, the response to auxin was inhibited by these antibodies, and the addition of maize ABP to the protoplasts increased auxin sensitivity [20"]. This suggests the ABPs have a physiological role in auxin reception. The kinetics of antibody inhil)ition indicated that the active site was the plasma membrane. Anti-idiotypic antibodies should prove useful because tile)' l)resumably recognize the auxin-binding site [21.]. Indole-3-acetic acid (IAA) specifically competed with these antibodies for ABP binding; therefore tile antibodies should block LeA-binding in physiological studies of ABPs. Several compounds other than the classic plant hormones have recently been identified as signal molecules. Oligosaccharides elicit several plant responses inclucling morphogenesis [22%23]. Purified oligogalacturonides of a discrete size range induced tobacco thin-layer cultures to flower [23] and caused ion fluxes across cell membranes [24]. Nevertheless, a role for oligosaccharides in normal plant development is still not clear. Extracellular glycoproteins also appear to have developmental signif-
Cell interactions in plants Becraft, Freeling 573 icance. For example, cell suspension cultures contain secreted proteins which can influence the development of other cells that are subsequently cultured in the same medium (reviewed in [25]). Antibodies directed against proteins secreted into carrot suspension cultures recognize arabinogalactan proteins in the plasma membrane and cell walls [26]. In roots, proteins recognized by these antibodies are expressed transiently in a dynmnic pattern that predicts the site of pericycle and xylem differentiation [26]. Other arabinogalactan epitopes are dyn,'mlically expressed during embryogenesis and flower development [27]. The authors suggest that these cell surface epitopes are involved in, or at least reflect, cell interactions during pattern establishment [26,27]. A number of signal molecules have been identified as part of the plant response to wounding or pathogenic attack. The first proven plant peptide signal was identified in the wound response [28"°]. Other wound signal molecules include salicylic acid, for which a binding protein has recently been identified [29], and jasmonic acid, which is a volatile, lipid-derived compound [30]. Thus many classes of compounds can elicit cellular responses and it is reasonable to expect a similar range of compounds in developmental signaling.
Cytoskeletal interconnections? The cytoskeleton controls the division plane in plant cells (reviewed in [36] ) and adjacent plant cells can influence each other's division planes [36]. Therefore, neighboring cells can affect one another's cytoskeletons, either directly or indirectly. Direct connections were suggested by experiments in which premitotic nuclei shifted position when adjacent cells were laser ablated [37"]. These nuclei were anchored across the vacuole by microtubulecontaining ,cytoplasmic strands under tension [37"]. The neighboring ceil apparently influenced the position of these anchoring strancls. It is possible that adjacent plant cells also interact via a mechanism similar to an extracellular matrix, which plays a major role in animal cell interactions and connects with the cytoskeleton. Although this notion is not widely entertained, several recent reports have shown that plants contain material cross-reactive to antibodies for extracellular matrix proteins involved in cell adhesion and cTtoskeletal anchoring. Human vitronectin antibodies recognize proteins in monocotyledons and dico~,ledons [38], and Fucu.~ contains proteins recognized by antibodies to vinculin, integrin and vitronectin [39].
Biophysical cell interactions Intercellular connections Plasmodesmata Plant cells are bounded by cell walls and consequently membranes of adjacent cells contact only at intercellular connections called plasmodesmata (reviewed in [31]). Because plasmodesmata form cytoplasmic connections between cells, they are believed to be important in cell-cell communication. Although plasmodesmata have a generalized structure, variations exist [31,32]. In leaves of the C4 plant sugarcane, structural differences in plasmodesmata depend on which cell types are being connected [32]. These cells have different requirements for the transport of metabolites between them, and this probably relates to the structural differences in plasmodesmata. Two approaches have been taken to study components of plasmodesmata. The first is based on similarities between plasmodesmata and gap junctions of animals, such as size exclusion limit and modulation by Ca 2+ [31]. A cDNA has been isolated that encodes a plant protein which cross-reacts with antibodies to the gap-junction protein connexin-32, which is derived from rat liver [33 ° ]. The deduced amino-acid sequence predicts chemical similarities with other connexins and thus suggests that it may function similarly in plants. Another study has identified proteins in maize that cross-react with antibodies to connexin-32 and connexin-43, from rat [34"]. Immunoelectron microscopy localized the connexin-43-1ike protein over the entire length of the plasmodesmata, and the comlexin-32-1ike protein mainly to the neck region [34°']. The second approach utilizes the tobacco mosaic virus movement protein that interacts with and alters the function of plasmodesmata [35]. This potentially provides a means for identifying important plasmodesmatal proteins and probing their function.
Mechanical stresses The role of biomechanics in plant development is controversial. An extreme interpretation of the biomechanical models is that a plant is like a balloon, with the internal tissue providing the driving pressure, and morphogenesis controlled by patterns of stress, reinforcement and weakness in the epidermis. The transition of the Anagal/is meristem from vegetative to floral development has recently been described in similar terms [40]. However, exanlples of genetic mosaic analyses where morphogenesis is controlled by the genotype of internal tissue discount the relative importance of the epidermis in organogenesis. In periclinal graft chimeras where the internal cells are Solanum &ciniatum, a lobed leaf species, and the epidermis is Nicotiana tabacum, an unlobed species, leaf shape corresponds to the internal cell genotype [41]. A recent study, although not directly addressing this topic, has unequivocally proved that such a mechanism is not responsible for gravitropic root bending. Although entire epidermis was removed from young maize roots, gravitropic bending was normal [42]. Therefore, differential growth was a whole organ response, and not controlled by the epidermis. While epidermal stress patterns appear not to direct morphogenesis, mechanical stresses may still influence development. Applied mechanical stress is capable of reorienting cortical micrombule arrays [43] and activating stretch-induced ion channels (reviewed in [44]), either of which could have developmental consequences. A biophysical model has also been used to explain correlations between the orientation of initial cells and the basic symmetry of the resultant organs [2°]. It was proposed that the initials act as a structural template for a primordium, and that this basic structure self-perpetuates during organ growth.
574
Patternformation and developmental mechanisms Electrical fields Plant cells generate endogenous electric currents d-mr have been implicated in cell interactions. Applied electricaJ currents about tenfold higher than endogenous currents caused a repolarization of the endogenous current to match dae applied current [45]. Exogenous electrical fields can also reorient cortical microtubules in plant cells [43]. These results suggest that cells within a tissue may coordinate their polarity through a collectively generated electric field.
Conclusions Tim field of plant cell interactions is still in its infancy. Plant cells interact through diverse mechanisms and on different levels, from fields of stress and electric',.d current to specific recognition of pollen grains. The self-incompatibility genes are the only genes specific,tlly involved in cell interactions that have been analyzed molecularly, and the mechanism of pollen recognition is still not clear. In the near future, the analysis of genes invoh,ed in cell interactions within the plant body should provide clues as to the nature of these interactions. Plant cells have proteins that are imnaunolo~cally related to proteins of gap junctions and the extracellular matrix o f animal cells, but a functional relationship remains to be demonstrated. Genetics has proven a powerful tool for identifying and anal)7.ing genes involved in cell interactions in animals and this is also likely to be the case in plants. At this point in time, either proper mutant screens have not been devised, or the mutmaLs have not yet been recognized as cell signaling mutants. Many genes invoh,ed in cell interactions are likely to be fundanaenta] to plant development ~md as such may be elucidated through the application of embryo mutant screens [46-,47].
Acknowledgements The :.lUthors thank lan Sussex Kelh" Dawe and .Iohn Fowler for critical reading of this ntanuscript.
References and recommended reading Papers of particul:lr interest, published within the annu-d period of review, have been highlighted as: • of special interest •• of outstanding interest 1. • A clear several
IRISH \rF: Cell Lineage in Plant Development. Czo'r Opin Genet Det' 1991, 1:169-173. summaw o f fate mapping experiments on apical meristems of plants. The importance of cell interactions is also stressed.
2.
DAWE RK, FREEUNG M: Cell Lineage and its Consequences in Higher Plants. P&nll 1991, 1:3-8. thorough treatment of the different techniques used in clonal analyses, and the information each tc%'hnique has provided. Examples of mature organs maintaining the basic sTmmetry of their initials leads to the proposal that pattern may self-perpetuate from the 'template' of initials. 3.
STEEVESTA, SUSSEX IM: Patterns ht Plant Development, 2nd edn. New York: Cambridge University Press; 1989.
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COEN ES, MEYEROWrrZEM: The War of the Whorls: Genetic Interactions Controlling Flower Development. Nature 1991, 353:31-37.
A succinct review of the rapidly moving field of flower developmental genetics. The similarities in the control of floral morphogenesis between two distantly related species, Antirrhinum and Arabidopsis, is highlighted. 5.
GRAY JE, MCCLUI~ BA, BONIG I, ANDERSON MA, CLARKE AE: Action of the Style Product of the Self-incompatibility Gene of N i c o t i a n a a l a t a (S.RNase) on In Vitro-grown Pollen Tubes. Plan! Cell 1991, 3:271-283.
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N,VV,l~.t.l.A]-I JB, NISHIO T, NASRAI.leXHME: The Seff-incompatibilitT Genes of Brassica: Expression and Use in Genetic Ablation of Floral Tissues. ,,Inmt Ret' Plant Pl~l,siol Mol Biol 1991, 42:393-422.
7. •
SATO T, THORSNI:SS MK, KANI)e~'AMYMK, NISHIO T, HIRAI M, NAS~.IJAIIJB, NtL'~RAIJAHME: Activity of an S Locus Gene Promoter in Pistils and Anthers of Transgenic Brassica. Plant Cell 1991, 3:867-876. Expresskm of a ILglucuronidase reporter gent: with an S-locus gene pronloter indicates that the S-gene is expressed in the stigma and mmsmitting tract of pistils, and in the tapetum and pollen of anthers. 8. •.
STE'IN.IC, HO\VlYTI"B, I]O','ES DC, NASRAI.IAIIME, NASRALI.AHJB: Molecular Cloning of a Putative Receptor Protein Kinase Gene Encoded at the Self-incompatibility Locus of Brassica oleracea. Proc Nail Acad Sci I'S:l 1991, 88:8816-8820. A second gone from the S-locus has a predicted extracellular dom:dn similar to the secreted S-locus glycopmtein, and an intracellular protein kinase domain. It may be part of the signal transduction i)athway for selFincompatibility. 9.
13OYESDe. Cltl..'N CII, TAN'rlKANIANAT, ESCll JJ, NASRAU.',HJB: Isolation of a Second Slocus-related cDNA from Brassica olerace~ Genetic Relationships Between the S Locus and Two Related Loci. Genelic~ 1991, 127:221-228.
10.
BECRAI:'I"PW, BONG/,d~.I)-I)II:RCI:DK, SYI.VF.S'ITRAW, POETHIG RS, FRI':EIJNG M: The liguleless. 1 Gene Acts Tissue Specifically in Maize Leaf Development. Det' Biol 1990, 141:220-232.
11. ,,
BI..'CRAIq"PW, FREEUNGM: Sectors of liguleless- 1 Tissue Interrupt an Inductive Signal During Maize Leaf Development. Planl Cell 1991, 3:801-O7. Shows that the ligulelessl mutant sectors cause a non-alignment of the ligule across the sectors. This su,,kRests that the LG1 gene is required for the transmisskm of a signal that organizes the ligular region in maize leaves. 12. •.
OPIq+NIIEIMERDG, HI:R+~,b~.NPL SIVAKtT,~IARANS, ESCH J, MARKS MD: A m y b Gene Required tbr Leaf Trichome Differentiation in Arabidopsis is Expressed in Stipules. Ce// 1991, 67>i83-493. The GIABROtLS'I gene required I'(~r leaf trichome fornmtion is a n(1,b gene. A GL131 promoter directed [3-glucuronidase expression in stipules suggesting that this gene regulates a diffusible ['actor that induced trichome fornlation on leaves. 13.
SINHAN, HAKES: Mutant Characters of Knotted Maize Leaves are Determined in the Innermost Tissue Layers. Det, Biol 1990, 141:203-210.
lq. •,
VOUJ~ImCHTE, VEIT 13, SINItA N, HAKE S: The Developmental Gene Knotted. l is a Member of a Maize H o m e o b o x Gene Family. Nature 1991, 350:241-243. Presentation of the predicted honmodomains from the Knotted. 1 gene and two related cDNA sequences. This is the first demonstration of homeol)ox genes in plants. 15.
LANGDAU" JA, NEt.SON T: Spatial Regulation of Photosynthetic Development in C4 Plants. Trends Genet 1991, 7:191-196.
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\'(tANGJ-L, KLESSIG DF, BERRY JO: Regulation of C4 Gene Expression in Developing Amaranth Leaves. Plant Cell 1992, 4:173-184.
17.
KAGANML, SACHST: Development of Immature Stomata: Evidence for Epigenetic Selection of a Spacing Pattern. Det, Biol 1991, 146:100-105.
Cell interadions in plants Becraft, Freeling 18.
CROXDAI.EJ, SMm-I J, YANDELLB, JOHNSON JB: Stomatal Patterning in Tradescantia: an Evaluation of the Cell Lineage Theory. Dev Biol 1992, 149:158-167.
19.
JONESAM, PRASADPV: Auxin-binding Proteins and their Possible Roles in Auxin-mediated Cell Growth. Bioes,~o,s 1992, 14:43-48.
20. ••
BARBIER-BRYGOOH, EPHRIT1KHINE G, KLAMBT D, MAUREI. C, PALMEK, SCI-IELLJ, GUERN J: Perception of the Auxin Signal at the Plasma Membrane of Tobacco Mesophyll Protoplasts. Plant J 1991, 1:83-93.
In this work, protoplast auxin-sensitivity is correlated to the anlount of ABP in the cells, is increased by adding ABP to the cells, and is inhibited with anti-ABP antibodies. This demonstrates a physiological role for ABPs. 21. ,,
PR&SADPV, JONES AM: Putative Receptor for the Plant Growth Hormone Auxin Identified and Characterized by Anti-idiotypic Antibodies. Proc Nail Acad Sci USA 1991, 88:5479-5483. Anti-idiotypic antibodies presumal)ly recognize the attxin-binding site of ABPs and so should be a powerful tool for studying possible physiological roles for these proteins. 22. •
RYAN CA, FAI~U:.R EE: Oligosaccharide Signals in Plants: a Current Assessment. Annu Ret, Plant Ph3'siol Mol Biol 1991, 42:6514574. A thorough overview of the roles of oligosaccharides as signal molecules in plants. 23.
MARFAV, GOIJJN DJ, EBI~RIIARD S, MOHNI-N D, DAR\qI.I. A, ALBEILSHEhMP: Oligogalacturonides are Able to Induce Flowers to Form on Tobacco Explants. P l a n t J 1991. 1:217-225.
24.
MATHIEUY, KURKDJb\NA, XIA H, GUERNJ, KOIJ.ERA, SPIRO /rID, O'NEILl. M, AI.BERSHFIM P, DAR\qlJ. A: Membrane Responses Induced by Oligogalacturonides in Suspension-cultured Tobacco Cells. Plant J 1991, 1:333-343.
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27.
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PEARCEG, STRYDObl D, JOHNSON S, RYAN CA: A Polypeptide from Tomato Leaves Induces Wound-inducible Pruteinase Inhibitor Proteins. Science 1991, 253:895-898. A signal that induces protease inhibitor.,; near wotmd sites is found to be a small peptide. This is the first peptide signal molecule identified in plants.
A plant protein is immunologic:tlly related to mt liver connexin-32, which functions in gap junctions. The eDNA sequence predicts a protein with similar chemical properties to connexin-32 suggesting it may have a similar function. 34. •.
YAHAI.OM A, WARMBRODY RD, D',dRD DW, TRAUB O, REVEL J-P, WIIJ.ECKI: K, EPEI. BL: Maize Mesocotyl Plasmodesmata Proteins Cross-react with Connexin Gap Junction Protein Antibodies. Plant Cell 1991, 3:407-417. The presence of immunologically related proteins in plant plasmodesmata and animal gap junctions indicates that these intercellular connections may share homology as well as analogy. This will facilitate research on plasmodesmatal function. 35.
\VC'OLFS, DEOM CM, BEACHY AR, LUCA. '¢, \VJ: Plasmodesmatal Function is Probed Using Transgenic Tobacco Plants that Express a Virus Movement Protein. Plant Cell 1991, 3:5934504.
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37. •
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42.
B.]ORKMANT, CLEL,~D RE: Root Growth Regulation and Gravitropism in Maize Roots does not Require the Epidermis. Planta 1991, i85:34-37.
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HUSHJM, OVERALLRL: Electrical and Mechanical Fields Orient Cortical Microtubules in Higher Plant Tissues. Cell Biol hit Rep 1991, 15:551-560.
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SCHROEDERJl, THUIJ~Atl P: Ca 2+ Channels in Higher Plant Cells. Plant Cell 1991, 3:555-559.
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MINAMG, GOLDSWORTm' A: Changes in the Electrical Polarity of Tobacco Cells Following the Application of Weak External Currents. Planta 1991, 186:104-108.
28. ••
29.
CHENZX, KIJ':SSIG DF: Identification of a Soluble Salicylic Acid-binding Protein that may Function in Signal Transduction in the Plant Disease-resistance Response. Proc Natl Acad Sci USA 1991, 88:8179-8183.
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FAP~IEREE, RYANCA: Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-inducible Proteinase lnhibitors. Plant Cell 1992, 4:129-134.
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33. .
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46. ••
,',,t.x'~EttU, TORRES RUIZ RA, BERLE'rH T, MISERA S, JURGENS G: Mutations Affecting Body Organization in the Arabidopsis Embryo. Nature 1991, 353:402-407. Describes a well devised mutant screen that identifies nine genes involved in spatial ~t.,~pects of pattern formation in embtTogenesis. Analysis of such genes may provide information ms to how patterning is coordinated in plants. 47.
CLARKJK, SHERIDANWF: Isolation and Characterization of 51 Embyro-specific Mutations of Maize. Plant Cell 1991, 3:935-951.
PW Becngt, M Fmeling, Department of Plant Biology, 111 GPBB, University of California, Berkeley, California 94720, USA.
575
Plant cells interact during development through diverse mechanisms that range from genetically encoded signals to physical stresses. Pollen self-incompatibility is the best understood cell interaction in plants. Analysis of genes that appear to be involved in specific developmental signals, such as liguleless'l from maize and GLABROUS1 from Arabidopsis, will provide clues as to the nature of cell interactions in plant development. Recent data suggest that intercellular connections may be more similar in plants and animals than previously thought.
Current Opinion in Genetics and Development 1992, 2:571-575
Introduction
Experimental evidence of cell interactions
Plants are structurally simple as compared with animals and do not undergo complex morphogenetic movements. Nonetheless, plants must contend with problems of coordinating cellular growth and differentiation, cell recognition, and even cell migration. Clonal analysis shows that plant cells remmn pluripotent until relatively late in development; therefore cell interactions detem~ine the fate of most plant cells [1o,2o]. Our present knowledge of plant cell interactions is limited and mainly phenomenological. For example, cells in the meristem must interact to coordinate activity. Phyllotax3,, mitotic activity, patterns of gene expression and phase transitions -all require coordination among meristematic cells. Classic experiments where surgically bisected meristems reorganized into two complete meristems have demonstrated that meristems are functionally integrated [3]. Several genes controlling the transition to a floral meristem and the identity of floral organs have recently been isolated (reviewed in [4°']). Cell interactions must be required for the manifestation of the phenotypes these genes confer, and some indirect evidence suggests that tile floricaula gene may participate in cell communication [1°], but the way cells within a meristem communicate is still not understood.
This paper reviews work from the past year that is relevant to the subject of plant cell interactions. Emphasis is on cell interactions in higher plant development. Individ. ual topics are discussed briefly as this is a broad field. The is considerable information concerning host-pathogen interactions in plants will not be covered.
Pollen-pistil interactions The clearest examples of cell interactions in plants are those between pollen and the pistil. The pollen and stigma must recognize compatible pollinations, and then file pollen tube migrates through the transmitting tissue of the pistil to the embryo sac where fertilization occurs. This has mostly been studied in self-incompatible plants. Self-incompatibility ensures outcrossing by preventing pollination of a flower by pollen of the same genotype. In gametophytic incompatibility, pollination is blocked if the haploid pollen carries either of the two S-alleles carried by the diploid stigmatic tissue. In Nicc~ tiana alata, the S-locus encodes a glycoprotein RNase that can enter the cytoplasm of in vitro grown pollen and inhibit protein synthesis [5]. This effect was, however, seen for both compatible and incompatible allelic combinations of S-RNase and pollen thus suggesting that other factors may be involved in vivo. In sporophytic self-incompatibility systems such as that occurring in Brassica, pollen germination is inhibited if file stigma carries either of the two S-alleles carried by the diploid pollen parent, regardless of the genotype of the pollen per se (reviewed in [6]). Polymorphisms in the S-locus glycoprotein (SLG) gene strongly correlate with the pollen incompatibility phenotype. Fusion of the SLG promoter to a [B-glucuronidase (GUS) reporter gene showed that SLG was expressed, as expected, in the stigma and transmitting tract of the style and also in the tapetum, which acts as a nurse tissue for developing pollen [7"]. SLG alone does not, however, appear to confer a self-incompatibility phenotype in transgenic
Abbreviations ABP--auxin-binding protein; glbT--glabrousl; GUS~-glucuronidase; IAA--indole-3-acetic acid; Igl--ligulelessl; SLG--S-Iocus glycoprotein; SRG--S-related genes.
(~) Current Biology Ltd ISSN 0959-437X
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Pattern formation and developmental mechanisms plants [8°-]. Several S-related genes (SRG) have been identified both linked and unlinked to tile S-locus [9]. An SRG that is tightly linked to, and presumed to reside at, the S-locus was cloned and encodes a putative receptor kinase, based on predicted mnino-acid sequence [8,°]. Transcripts from this gene were detected exclusively in pistils and anthers, and analysis of several alleles showed a high degree of polymorphism. This suggests that the receptor kinase m W have a role in self-incompatibility.
Cell interactions in leaf development Recent studies have identified cell interactions invoh,ed in coordinating leaf differentiation. Maize leaves consist of the morphologically distinct blade and sheath. These join at the ligular region that consists of a tissue fringe called tile ligule and two triangnlar structures called auricles, which act as a hinge. Recessive ligulelessl (Igl) mutants lack ligules and auricles. In genetic mosaics, the wild-type Lgl allele acts autonomously although tile wildtype mesophyil can induce a rudimentary ligule in mutant epidermis directly overlaying it [10]. Furthemlore, when lgl mutant sectors interrupted the ligule, they caused the ligule on the marginal side of the sector to be displaced basipetally relative to the ligule on the other side of the sector [11-]. This suggested a model in which the mutant sectors blocked the transmission of a signal that organizes the ligular region, thus causing a delayed ligule initiation on the marginal side. Because leaf differentiation proceeds basipetally, this delay resulted in a more basal ligule position. Thus die LGI gene appears to be required for reception or transmission of this signal. In Arabidops& glabrousl (glbl) mutants lack the hairlike epidermal trichome cells on leaves, petioles, sepals and stems, and appear to have no other defect. The DNA sequence of this gene encodes a protein with a Myb DNAbinding domain [12-.]. The GLB1 promoter was fused to a GUS reporter gene and transformed into wild-type Arabidopsis. No expression was detected in trichomes; GUS staining occurred only in stipules, small appendages at the base of leaves [12-]. This suggests that GLB1 regulates the production of a diffusible factor in stipules that induces trichome fom~ation in other organs. A genetic mosaic analysis would be a more rigorous test of this hypothesis. The leaf vasculature has been implicated as having an organizational role during leaf development. Lateral veins of maize leaves are the site of action for dominant Knottedl mutations although other cells including epidermis are induced to divide [13]. Kp,ottedl was tile first plant homeobox gene identified [14-]. As such, Knottedl alters the development of veins which then appear to regulate epidermal cell divisions through cell interactions. Veins also appear central to the developmental anatomy of plants that exhibit C4-type photosynthesis. While C3 plants perform all their photosynthesis in a single cell type, C4 plants divide their photosynthetic reactions between mesophyll cells and vascular bundle sheath cells. These different photosynthetic cell types are arranged in a specialized organization called the Kranz anatomy [15]. In the blade of maize, veins are tightly packed and all mesophyll cells express C4 enzymes. In contrast, in
the sheaths and husk leaves, veins are widely spaced and mesophyll cells in close proximity to veins express C4 enzymes while at a distance dley express C3 enzymes. As such, the veins appear to produce a signal that induces C4 development. Although the nature of this signal is unclear, C4 gene expression is l)roperly compartmentalized from the outset of vascular differentiation, kal interesting new maize mutant, bundle sheath defective, has normal C4 mesophyll but the bundle sheath ceils fail to differentiate properly (JA Langdale, abstract 78, 34th Annual Maize Genetics Conference, Asilomar, California, March 1991). A lesion in the signaling mechmxism is a possible explanation for this phenotype. In tile dicotyledonous C4 Amaranthus, the C4 pattern of photosynthetic enzyme expression is not immediately expressed but becomes established after vascular differentiation [16]. Thus cells may interact somewhat differently in processes that are similar between monocots and dicots. A striking feature of leaf epidermis is the regular pattern of stomata. In Sansevieria leaves, many stomata arrest during development. The pattern of mature stomata is more regular than that of the immature stomata, suggesting that developing stomata interact with their surrounding tissue and that an epigenetic selection mechanism allows maturation ocdy of properly spaced stomata [17]. "Laser ablation of stomatal initials in similarly patterned D'adescantia leaves caused no change in stomatal pattern; however, deteru~inative events may have already occurred [18].
Signal molecules Auxins are the most studied of the classic phytohormones and are involved in many plant responses, both short- and long-range. The current challenge is to elucidate auxin receptors and signal transduction pathways (reviewed in [19] ). Auxin-binding proteins (ABPs) have been identified in the plasma membrane, endoplasmic reticulum, nucleus and cTtosol [19,20..,21.]. In tobacco protoplasts, sensitivity to auxin correlated with the amount of cross-reactivity to maize anti-ABP antibodies, the response to auxin was inhibited by these antibodies, and the addition of maize ABP to the protoplasts increased auxin sensitivity [20"]. This suggests the ABPs have a physiological role in auxin reception. The kinetics of antibody inhil)ition indicated that the active site was the plasma membrane. Anti-idiotypic antibodies should prove useful because tile)' l)resumably recognize the auxin-binding site [21.]. Indole-3-acetic acid (IAA) specifically competed with these antibodies for ABP binding; therefore tile antibodies should block LeA-binding in physiological studies of ABPs. Several compounds other than the classic plant hormones have recently been identified as signal molecules. Oligosaccharides elicit several plant responses inclucling morphogenesis [22%23]. Purified oligogalacturonides of a discrete size range induced tobacco thin-layer cultures to flower [23] and caused ion fluxes across cell membranes [24]. Nevertheless, a role for oligosaccharides in normal plant development is still not clear. Extracellular glycoproteins also appear to have developmental signif-
Cell interactions in plants Becraft, Freeling 573 icance. For example, cell suspension cultures contain secreted proteins which can influence the development of other cells that are subsequently cultured in the same medium (reviewed in [25]). Antibodies directed against proteins secreted into carrot suspension cultures recognize arabinogalactan proteins in the plasma membrane and cell walls [26]. In roots, proteins recognized by these antibodies are expressed transiently in a dynmnic pattern that predicts the site of pericycle and xylem differentiation [26]. Other arabinogalactan epitopes are dyn,'mlically expressed during embryogenesis and flower development [27]. The authors suggest that these cell surface epitopes are involved in, or at least reflect, cell interactions during pattern establishment [26,27]. A number of signal molecules have been identified as part of the plant response to wounding or pathogenic attack. The first proven plant peptide signal was identified in the wound response [28"°]. Other wound signal molecules include salicylic acid, for which a binding protein has recently been identified [29], and jasmonic acid, which is a volatile, lipid-derived compound [30]. Thus many classes of compounds can elicit cellular responses and it is reasonable to expect a similar range of compounds in developmental signaling.
Cytoskeletal interconnections? The cytoskeleton controls the division plane in plant cells (reviewed in [36] ) and adjacent plant cells can influence each other's division planes [36]. Therefore, neighboring cells can affect one another's cytoskeletons, either directly or indirectly. Direct connections were suggested by experiments in which premitotic nuclei shifted position when adjacent cells were laser ablated [37"]. These nuclei were anchored across the vacuole by microtubulecontaining ,cytoplasmic strands under tension [37"]. The neighboring ceil apparently influenced the position of these anchoring strancls. It is possible that adjacent plant cells also interact via a mechanism similar to an extracellular matrix, which plays a major role in animal cell interactions and connects with the cytoskeleton. Although this notion is not widely entertained, several recent reports have shown that plants contain material cross-reactive to antibodies for extracellular matrix proteins involved in cell adhesion and cTtoskeletal anchoring. Human vitronectin antibodies recognize proteins in monocotyledons and dico~,ledons [38], and Fucu.~ contains proteins recognized by antibodies to vinculin, integrin and vitronectin [39].
Biophysical cell interactions Intercellular connections Plasmodesmata Plant cells are bounded by cell walls and consequently membranes of adjacent cells contact only at intercellular connections called plasmodesmata (reviewed in [31]). Because plasmodesmata form cytoplasmic connections between cells, they are believed to be important in cell-cell communication. Although plasmodesmata have a generalized structure, variations exist [31,32]. In leaves of the C4 plant sugarcane, structural differences in plasmodesmata depend on which cell types are being connected [32]. These cells have different requirements for the transport of metabolites between them, and this probably relates to the structural differences in plasmodesmata. Two approaches have been taken to study components of plasmodesmata. The first is based on similarities between plasmodesmata and gap junctions of animals, such as size exclusion limit and modulation by Ca 2+ [31]. A cDNA has been isolated that encodes a plant protein which cross-reacts with antibodies to the gap-junction protein connexin-32, which is derived from rat liver [33 ° ]. The deduced amino-acid sequence predicts chemical similarities with other connexins and thus suggests that it may function similarly in plants. Another study has identified proteins in maize that cross-react with antibodies to connexin-32 and connexin-43, from rat [34"]. Immunoelectron microscopy localized the connexin-43-1ike protein over the entire length of the plasmodesmata, and the comlexin-32-1ike protein mainly to the neck region [34°']. The second approach utilizes the tobacco mosaic virus movement protein that interacts with and alters the function of plasmodesmata [35]. This potentially provides a means for identifying important plasmodesmatal proteins and probing their function.
Mechanical stresses The role of biomechanics in plant development is controversial. An extreme interpretation of the biomechanical models is that a plant is like a balloon, with the internal tissue providing the driving pressure, and morphogenesis controlled by patterns of stress, reinforcement and weakness in the epidermis. The transition of the Anagal/is meristem from vegetative to floral development has recently been described in similar terms [40]. However, exanlples of genetic mosaic analyses where morphogenesis is controlled by the genotype of internal tissue discount the relative importance of the epidermis in organogenesis. In periclinal graft chimeras where the internal cells are Solanum &ciniatum, a lobed leaf species, and the epidermis is Nicotiana tabacum, an unlobed species, leaf shape corresponds to the internal cell genotype [41]. A recent study, although not directly addressing this topic, has unequivocally proved that such a mechanism is not responsible for gravitropic root bending. Although entire epidermis was removed from young maize roots, gravitropic bending was normal [42]. Therefore, differential growth was a whole organ response, and not controlled by the epidermis. While epidermal stress patterns appear not to direct morphogenesis, mechanical stresses may still influence development. Applied mechanical stress is capable of reorienting cortical micrombule arrays [43] and activating stretch-induced ion channels (reviewed in [44]), either of which could have developmental consequences. A biophysical model has also been used to explain correlations between the orientation of initial cells and the basic symmetry of the resultant organs [2°]. It was proposed that the initials act as a structural template for a primordium, and that this basic structure self-perpetuates during organ growth.
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Patternformation and developmental mechanisms Electrical fields Plant cells generate endogenous electric currents d-mr have been implicated in cell interactions. Applied electricaJ currents about tenfold higher than endogenous currents caused a repolarization of the endogenous current to match dae applied current [45]. Exogenous electrical fields can also reorient cortical microtubules in plant cells [43]. These results suggest that cells within a tissue may coordinate their polarity through a collectively generated electric field.
Conclusions Tim field of plant cell interactions is still in its infancy. Plant cells interact through diverse mechanisms and on different levels, from fields of stress and electric',.d current to specific recognition of pollen grains. The self-incompatibility genes are the only genes specific,tlly involved in cell interactions that have been analyzed molecularly, and the mechanism of pollen recognition is still not clear. In the near future, the analysis of genes invoh,ed in cell interactions within the plant body should provide clues as to the nature of these interactions. Plant cells have proteins that are imnaunolo~cally related to proteins of gap junctions and the extracellular matrix o f animal cells, but a functional relationship remains to be demonstrated. Genetics has proven a powerful tool for identifying and anal)7.ing genes involved in cell interactions in animals and this is also likely to be the case in plants. At this point in time, either proper mutant screens have not been devised, or the mutmaLs have not yet been recognized as cell signaling mutants. Many genes invoh,ed in cell interactions are likely to be fundanaenta] to plant development ~md as such may be elucidated through the application of embryo mutant screens [46-,47].
Acknowledgements The :.lUthors thank lan Sussex Kelh" Dawe and .Iohn Fowler for critical reading of this ntanuscript.
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