Structure, Delimitation, Nomenclature and Classification of Stomata

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1 Acta Botanica Sinica 2004, 46 (2): Structure, Delimitation, Nomenclature and Classification of Stomata Malvey PRABHAKAR (Plant Anatomy and Taxonomy Laboratory, Department of Botany, Osmania University, Hyderabad , India) Abstract: The paper reviews stomatal types observed in 500 species of angiosperms besides those described in the literature and deals with the problems of their structure, delimitation, nomenclature and classification. In view of the varied definitions available in the literature for subsidiaries, stomatal types and, the definition and delimitations being variously interpreted by different workers, a modified definition for the subsidiaries and stomata is presented. In accordance with the international code of nomenclature for plants, the names of the stomata widely in use are retained (rule of priority). They have been presently classified as pericytic, desmocytic, paracytic, diacytic, anisocytic, anisotricytic, isotricytic, tetracytic, staurocytic, anomocytic, cyclocytic and a good number of varieties under each type are presented. These stomatal types are recognised on the basis of their structure rather than its ontogenetic pathways. Key words: classification; definition; plant stomata The early history of stomatal nomenclature dates back to Prantle (1872; 1881). Subsequently several classificatory systems have come into existence, which are mostly based on ontogeny ( Florine, 1931; 1933; Pant, 1965; Payne, 1970; 1979), or combination of structure and ontogeny (Paliwal, 1969b; Fryns-Claessens and van Cotthem, 1973; Stevens and Martin, 1978). Though several classificatory systems and review works (Vesque, 1889; Francey, 1936; Metcalfe and Chalk, 1950; Metcalfe, 1961; Stace, 1965; van Cotthem, 1970b; Dilcher, 1974; Patel, 1979; Rasmussen, 1981; Kidwai, 1981; Inamdar et al., 1986; Baranova, 1987; 1992) have been published, we lack precise definition for subsidiaries and stomatal types. Francey (1936) recognised eight categories and 34 structural stomatal types based on the number, position and size of the subsidiaries. Though his classificatory system was fairly good but it was not used by subsequent workers. Survey of the literature reveals that the most widely accepted and used stomatal classificatory system based on the mature stomatal structure is that of Metcalfe and Chalk s (1950), Metcalfe (1961) and Stace (1965). While using their classificatory systems some strictly followed the definition of the subsidiaries and delimit the stomata, while others do not (Prabhakar and Leelavathi, 1992 ). For example, though the stomata of Lathyrus (Simola, 1968), which may normally be considered as paracytic on the basis of orientation of the two surrounding cells in relation to the guard cells, following strictly the definition of Metcalfe and Chalk (1950), they have been classified under anomocytic by Simola (1968), because of the indistinct nature of the abutting cells. However, Stace (1965) has named such stomata as paracytic. Metcalfe and Chalk (1950) also did not seem consistent in applying their definition of subsidiaries throughout their book. For example the stoma represented in Figs.1788, 2220, 3098 (Metcalfe and Chalk, 1950) are surrounded by two parallel indistinct cells and hence should be assigned to anomocytic stomata sen. str. Metcalfe and Chalk (1950). The authors however described them as paracytic stomata. While others classified such stomata having four or more abutting cells into paracytic stomata (Paliwal, 1961; Inamdar, 1968; 1970; Fryns-Claessens and van Cotthem, 1973; Wilkinson, 1979; Kidwai, 1981) and a stoma having only two abutting cells/subsidiaries parallel to the guard cells have been designated as hemiparacytic, parallelocytic Eupara-twi-monocyclic, obliparatwimonocyclic, duplo-para-tetra-bicyclic, para-polycyclic, para-spirocyclic, etc. (Patel, 1979; Wilkinson, 1979). The classificatory systems provided subsequent to Metcalfe and Chalk (1950), Metcalfe (1961) and Stace (1965), I do not feel at all an improvement over the concept of Metcalfe and Chalk (1950). In these new classifications several new terms which the authors themselves were not able to use them in strict sense in their subsequent publication for describing the stomata have been introduced. The draw back of all these classificatory systems including that of Metcalfe and Chalk (1950 ) mainly lies in the definitions of subsidiaries and partly the definitions of stomatal types. Further several researcher have provided different definitions for a single type of stomata. Some of these definitions for paracytic stomata are listed below: Vesque (1889): Stomata with two subsidiary cells parallel to the long axis of the pore-rubiaceous (*Figs.1 10). Received 10 Oct Accepted 7 Jul. 2003

2 Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata Solereder (1908): The pair of the guard cells are accompanied on either sides (i.e. to the right and left) by one or more subsidiary cells, which are placed parallel to the pore- Rubiaceous type (*Figs.1 5, 7, 9, 10, 13 16). Francey (1936): Stoma surrounded by two parallely oriented cells which may be equal or unequal, designated as types 3 and 4 respectively (*Figs.1 3, 11, 12 ). Metcalfe and Chalk (1950): Stoma accompanied on either sides by one or more subsidiary cells (cells distinct from other epidermal cells) parallel to the long axis of the pore and guard cells-paracytic type (*Figs.1 5, 7, 9, 10, 13 16). Stace (1965): Stoma with two subsidiary cells lying parallel to the guard cells-paracytic (Figs.1 10). Figs Diagrammatic representation of the so called paracytic stomata Stomata surrounded by distinct or indistinct subsidiaries. 25, 26. Stomata with distinct subsidiaries. 27, 28. Stomata with indistinct subsidiaries Subsidiaries dicyclic. 34, 35. Stomata with distinct crystalliferous subsidiaries. 36. Stomata with one distinct and the other indistinct subsidiary Pericytic stomata. 37, 38. Stomata with distinct or indistinct subsidiary. 39, 40. Subsidiary transversly oriented to guard cells. 41, 42. Subsidiary parallel to guard cells. 43, 44. Subsidiary oblique to guard cells Subsidiaries 1 1/2 cyclic Subsidiaries dicyclic Subsidiaries tricyclic. *, figures cited here fit into the definition given by the respective authors.

3 Cronquist (1968): Stoma with two equal subsidiary cells flanking the guard cells-paracytic stomata (*Fig.1). Fahn (1969): Each guard cell is accompanied by one or more subsidiary cells, the longitudinal axis of which are parallel to that of the guard cells and aperture-rubiaceous or Paracytic type (*Figs.1 5, 7, 9, 10, 13 16). Paliwal (1969a): Two or more subsidiary cells flank the stomata parallel with long axis of the guard cells-paracytic stomata (*Figs.1 5, 13, 14, 16 ). Rajagopal (1973): Abutting subsidiaries two, parallel to the guard cells, distinct or indistinct, with or without conjoint walls towards one or both poles-a Diacytic type (*Figs.1 5, 7, 9 12, 15, ). Note: When the two subsidiaries are without conjoint walls towards one or both poles of the guard cells, it is bound to leave a space which will be abutted by one or more cells as also illustrated by the same author (Figs.18 21). Dilcher (1974): One or two cells adjacent to the guard cells with their long axis parallel to the long axis of the guard cells-paracytic type (*Figs.1 4, 7, 9 12, 15, 17 22). Cutter (1978): One or more (often two) subsidiary cells are present, with their long axis parallel to the guard cells- Paracytic (*Figs.1 10, 13 17). Esau (1979): One or more subsidiary cells border the stoma parallel with the long axis of the guard cells- Paracytic type (*Figs.1 10, ). Wilkinson (1979): Stoma accompanied on either side by one or more subsidiary cells parallel to the long axis of the pore and guard cells. The subsidiaries may or may not meet over the poles and may or may not laterally elongate- Paracytic type (*Figs.1 5, 7, 9, 10, 13 16, 19, 20, 23, 24). Following strictly the above definitions the stomata represented in Figs.1 24 can be accommodated under the so called paracytic ones. A New Classification and Modified Definitions It is clear from the above introduction that the definitions provided by various workers for different stomatal types, are ambiguous. In order to remove the ambiguity the author felt the necessity to redefine the subsidiaries and stomatal types which is presented below based on his observations on more than 500 species of angiosperms (for details of the species c.f. Anna Mani & Prabhakar, 1991a; 1991b; 1993; 1994a; 1994b; 1995; Anna Mani et al., 1993; Bhatia et al., 1986; 1988; Ferzana et al., 1991; 1994a; 1994b; Jelani and Prabhakar, 1991; 1992; 1993; Jelani et al., 1990; 1991; 1993; Koteswar Rao et al., 1988; Leelavathi and Ramayya, 1975; Leelavathi et al., 1980; 1981; 1984a; 1984b; 1985; 1988a; 1988b; Padma Rao et al., 1988; Prabhakar and Anna Mani, 1995; 1996; Prabhakar and Leelavathi, 1989; 1991;1992; Prabhakar and Ramayya, 1975; 1979; Prabhakar et al., 1984; 1985;1986; 1988a; 1988b; 1988c; 1990; Ramayya and Prabhakar, 1973; 1975; Ramayya et al., 1983; Rao et al., 1991; 1992a; 1992b; 1992c, 1993a; 1995; Verma et al., 1989; 1991; 1992; Vijay Kumar et al., 1986) and also the information available in the literature. Stomatal pore: An opening in the epidermis surrounded by a pair or more guard cells. Stoma: Stomatal pore and a pair of guard cells. Stomatal complex: Stoma surrounded by subsidiaries (stomatal types). Subsidiary cells * : Cells surrounding a pair of guard cells in one (Fig. 25) or more cycles (Fig.26); subsidiaries of the cycle abutting on stoma may (Figs.25, 26, 34 36) or may not be distinct from the adjacent epidermal cells ( Figs. 27, 28 ), but of the other cycle(s) when present are morphologically distinct (Fig. 26). The subsidiaries of the outer cycle may (Fig. 26) or may not coincide with those of the abutting cycle in number, arrangement and orientation, etc. (Figs ). The term subsidiary is restricted to mature stomata only. The subsidiaries of the abutting as well as other cycle (s) may be perigynous or mesogenous in origin and can be referred as perigene and mesogen cells (while describing the ontogeny) depending upon their origin. A subsidiary derived from stomatal meristemoid need not be distinct at maturity from other epidermal cells. Similarly a subsidiary not derived from stomatal meristemoid ( i.e. perigene ) may be distinct from other epidermal cells or other subsidiary cells. Pericytic stomata: Stoma (pair of guard cells) surrounded *, cells abutting the stoma has been designated as subsidiaries/auxillary cells when they are distinct from other epidermal cells and as annexes/surrounding cells/accessory cells/contact cells/ordinary cells when they are indistinct (Francey, 1936; Eames and Mc Daniels, 1947; Metcalfe and Chalk, 1950; Mc Lean and Cook, 1951; Fryns- Claessens and van Cotthem, 1973; Tomlinson, 1974; Patel, 1978; Cutter, 1978; Rasmussen, 1981). However the criteria to judge the distinctness has been mostly left to the subjective judgement. In retrospect the criteria used for distinctness by various workers are morphological (shape, size, anticlinal walls and surface), cytological (density of cytoplasm, size of the nucleus, presence or absence of plastids and ergastic substances) (Figs.34 36), number, position, orientation, physiological and ontogenetical (Patel, 1978; Stevens and Martin, 1978). Tracing cytological, physiological and ontogenetical characters in the herbarium and fossil materials is impracticable. All the cells abutting the guard cells are distinct from the other epidermal cells by virtue of their position (i.e. abutting nature to the guard cells) hence prefer to call them subsidiaries.

4 Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata by a single distinct or indistinct subsidiary cell (Figs ). The subsidiary cell may be variously oriented to the guard cell and may be monocyclic ( Figs ), 11/2 cyclic ( Figs ), di-, tri- to polycyclic ( Figs ). Synonyms: Adetostomy, amphipericytic, co-pericytic, coperi-desmo-twi-bicyclic, coperi-polohemibicyclic, copoloperi-hemibicyclic, duplopericytic, double floating, duploperi-twi-bicyclic, floting, pericytic, pyrosia type, perihaplo-monocyclic, Ringzellen-type, stomata libera, unizyklisch (Prantle, 1881; Maroti, 1961; Mickel, 1962; Figs Desmocytic stomata. 63. Stomata with distinct subsidiary. 64. Stomata with indistinct subsidiary. 65, 66. Subsidiary transversely oriented to guard cells. 67, 68. Subsidiary parallelly oriented to guard cells. 69, 70. Subsidiary obliquely oriented to guard cells Subsidiaries 1 1/2 cyclic Subsidiaries dicyclic. 90. Subsidiaries tricyclic Paracytic stomata. 91. Stomata with distinct subsidiaries. 92. Stomata with indistinct subsidiaries Subsidiaries parallel to the guard cells Subsidiaries transverse to guard cells Subsidiaries oblique to guard cells Subsidiaries 1 1/2 cyclic Subsidiaries dicyclic Subsidiaries hemitricyclic Subsidiaries tricyclic.

5 Mickel and Lersten, 1967; van Cotthem, 1970a, 1970b; Probst, 1971; Dilcher, 1974; Patel, 1979). Desmocytic: A stoma completely surrounded by a single distinct or indistinct cell with a conjoint wall. The subsidiary cell may be variously oriented to the guard cells and the conjoint wall may be variable in position. The subsidiaries may be monocyclic ( Figs ), 1 1/2 cyclic, di-, trito polycyclic (Figs.71 90). Synonyms: Codesmoperi-twi-bicyclic, codesmo-polohemibicyclic, copolo-desmo-hemibicyclic, desmocytic, desmo-haplo-monocyclic, duplodesmo-twi-bicyclic, hanging or suspended stomates, stomata suspensa (Mickel and Lersten, 1967; van Cotthem, 1970a; 1970b; Dilcher, 1974; Patel, 1979; Prantle, 1881) or indistinct (Figs ), equal or unequal (Figs ), parallel (Figs ), transverse (Figs ) or obliquely oriented (Figs. 102,103 ) to the guard cells, but their conjoint walls are towards the poles of the guard cells. The subsidiaries may be mono- to polycyclic (Figs ). Note: Francey (1936) recognised two types of stomata under this category based on the size of subsidiaries. Type 1 is represented by more or less equal sized subsidiaries (Figs.91, 92). Type 2 by unequal sized subsidiaries (Figs. 91,92). These can be now recognised as varieties under the type paracytic only. Similarly the stoma having distinct or indistinct subsidiaries, parallel oblique or transversely oriented subsidiaries can be recognized into different varieties. Synonyms: Allelocytic, amphiparacytic, bicyctic paracytic, duplo-para-tetra-bicyclic, eupara-twimonocyclic, laterocytic oblipara-twimonocyclic, paracytic, parallelocytic, para-polycyclic, paraspirocyclic, rubiaceous (Vesque, 1889; Metcalfe and Chalk, 1950; Payne, 1970; Guyot, 1971; Dilcher, 1974; Hortog and Bass, 1978; Patel, 1979). Diacytic stomata: A stoma completely surrounding by only two distinct or indistinct subsidiaries (Figs.123, 124), equal or unequal (Figs ), parallel (Figs. 127, 128), transverse (Figs. 129, 130) or obliquely oriented (Figs. 131, 132 ) to the guard cells, but the conjoint wall of the abutting subsidiaries are lateral to the guard cells. The subsidiaries may be monocyclic to polycyclic ( Figs ). Note: Francey (1936) recognised two types of stomata under this category also, based on equal ( Figs. 123, 124 ) or unequal sized subsidiaries (Figs.125, 126). These can be recognised as varieties under the diacytic stomata only. Similarly a stoma having distinct or indistinct subsidiaries, transversely, obliquely or parallelly oriented subsidiaries can be recognised into different varieties. Synonyms: Amphidiacytic, axillocytic, bicyclic diacytic, caryophyllaceous, coaxilocytic, coparirtocytic, copolocytic, diacytic, diallelocytic, diapolocyclic, diapolycyclic, diaspirocyclic, diatwi-monocyclic, duplodia-tetra-bicyclic, labiateous, oblidia-monocyclic, perietocytic, polocytic, polohaplo-acyclic, polycytic, pteris type, stomata applicata, stomata adnata (Prantle, 1881; Vesque, 1889; Giesenhagen, 1901; Metcalfe and Chalk, 1950; Payne, 1970; van Cotthem, 1970a; 1970b; Guyot, 1971; Probst, 1971; Dilcher, 1974; Patel, 1979). Anisocytic stomata: A stoma completely is surrounded by only three subsidiaries, variable in position and shape, but one of the subsidiary is distinctly small (Figs ). The subsidiaries may be mono- to polycyclic (Figs ). Synonyms: Amphianisocytic, anisocytic, aniso-trimonocyclic, axillocytic, coaxillocytic, cruciferous, helicocytic, helico-spirocyclic obli-haplo-acyclic (Vesque, 1889; Metcalfe and Chalk, 1950; Payne, 1970; Dilcher, 1974; Patel, 1979). Anisotricytic stomata: A stoma completely surrounded by only three subsidiaries, variable in position and shape, but one of the subsidiary is distinctly large. The subsidiaries may be mono- to polycyclic (Figs ). Synonyms: Anisocytic, anomocytic, helicocytic, diacytic ( Metcalfe and Chalk, 1950; Stace, 1965; Wilkinson, 1979 ). Isotricytic stomata: A stoma completely surrounded by only three subsideries, variable in position and shape,but the three subsidiaries are more or less of equal size. The subsidiaries may be mono- to polycyclic ( Figs ). Synonyms: Anomocytic (Metclafe and Chalk, 1950; Stace, 1965). Note: Francey (1936) recognised seven types under the above three categories (i.e. stoma surrounded by three cells), based on the size and position of the subsidiary cells. The definitions of some of these types and figures represented are overlapping. Hence presently they are divided into three categories of stomata which are structurally distinct from one another, i.e. anisocytic, isotricytic and anisotricytic. Under each of these categories a good number of varieties can be recognised based on the shape, size, structure of inner and outer cycles of the subsidiaries. Tetracytic stomata: Stomata completely surrounded by only four subsidiaries, of variable size and shape, of which two are polar and two lateral in position. The subsidiaries may be mono- to polycyclic (Figs ). Synonyms: Anphibrachiparatetracytic, amphiparatetracytic, angiopteris type, bicytic paracytic, brachyparahexacytic, brachyparatetracytic, cyclocytic, duplo-para-tetraacyclic, grass type, hemidiahaplo-acyclic, hemiparacytic,

6 Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata hemipara-haplo-acyclic, hexacytic, hexa-a-hemibicyclic, hexa-bhemibicyclic, obli-tri-acyclic, obli-twi-acyclictetracytic, palm type, paracytic, parahexacytic, paratetracytic, para-twi-acyclic, quadricytic, rubaceous, staurocytic, stomata quadricellulaires, tetra cyclocytic, tetracytic, tetramonocyclic, tricyclic (Vesque, 1889; Metcalfe and Chalk, 1950; Maroti, 1958; Prat, 1960; Metcalfe, 1961; Stace, 1965; van Cotthem, 1970b; Guyot, 1971; Dilcher, 1974; Tomlinson, 1974; Patel, 1979; Wilkinson, 1979). Staurocytic stomata: Stoma completely surrounded by only four subsidiaries, variable in shape and size but two of their conjoint walls polar, while the other two are lateral to guard cells. The subsidiaries may be mono to polycyclic (Figs ). Figs Diacytic stomata. 123, 124. Stomata with distinct and indistinct subsidiaries respectively. 125, 126. Stomata with unequal subsidiaries. 127, 128. Subsidiaries parallel to guard cells. 129, 130. Subsidiaries transverse to guard cells. 131, 132. Subsidiaries oblique to guard cells. 133, 134, , 145, 146. Subsidiaries 1 1/2 cyclic , 143, 144, 147. Subsidiaries dicyclic Anisocytic stomata Stomata with indistinct subsidiaries. 149, 150. Stomata with distinct subsidiaries Stomata with one or two distinct subsidiaries Subsidiaries 1 1/2 cyclic Subsidiaries dicyclic Anisotricytic stomata Stomata with indistinct subsidiaries. 166, 167. Stomata with distinct subsidiaries. 168, 169. Stomata with one or two distinct subsidiaries Subsidiaries 1 1/2 cyclic Isotricytic stomata. 171, 172. Stomata with indistinct and distinct subsidiaries respectively. 173, 174. Stomata with one or two distinct subsidiaries.

7 Synonyms: Type 15, stauro-cyclocytic, staurocytic, stauro-tetra-monocylic (Francey, 1936; van Cotthem, 1970a; 1970b; Dilcher, 1974; Patel, 1979; Wilkinson, 1979 ). Anomocytic stomata: Stoma surrounded by four or more subsidiaries, variable in position, shape and size ( other than tetracytic and staurocytic types; Figs ). Synonyms: Actinocytic, amphibrachyparacytic, anomocytic-polycytic, brachyparacytic, hemiparacytic, latero-twi-acyclic, oblitwi-acyclic, paracytic, stephanocytic, termino-twi-acyclic (Dilcher, 1974; Patel, 1979; Wilkinson, 1979; Baranova, 1987). Cyclocytic stomata: Stoma is surrounded by four or more subsidiaries, variable in position, shape and size but arranged in a narrow ring ( Figs ). Note: A desmocytic (Fig. 37), pericytic (Fig. 63), paracytic (Fig. 91), diacytic (Fig.123 ), anisocytic (Fig. 149 ), isotricytic (Fig.172 ), anisotricytic ( Fig.167 ), staurocytic ( Fig.187) and tetracytic stoma (Fig.175), having one to four subsidiaries arranged in a narrow ring are not included under cyclocytic stomata. Synonyms: Amphicyclocytic, angiopteris type, cyclocytic, cyclo-multi-monocyclic, encyclocytic, hexamonocytic, multi-bicyclic, multi-polycyclic, polycytic (Shtromberg, 1956; Stace, 1965; Probst, 1971; Dilcher, 1974; Patel, 1979). Actinocytic, stephanocytic, actino-multi-monocyclic: I feel that identification of actinocytic stomata ( so also with other types like stephanocytic ) is a difficult problem Figs Tetracytic stomata. 175, 176. Stomata with distinct or indistinct subsidiaries respectively Stomata with one to three distinct subsidiaries. 182, 183. Subsidiaries 1 1/2 cyclic Subsidiaries dicyclic, hemitricyclic and tricyclic respectively Staurocytic stomata. 187, 188. Stomata with distinct and indistinct subsidiaries respectively Stomata with one to three small subsidiary cells Stomata with one to three large subsidiary cells Anomocytic stomata. 195, 196, 202, 203. Stomata with one, three or more radiating subsidiaries. 197, 199. Stomata with one distinct parallel subsidiary Stomata with two distinct parallel subsidiaries Subsidiaries hemidicyclic Subsidiaries parallel to guard cells Subsidiaries transverse to guard cells Some subsidiaries parallel to guard cells while other radiating Cyclocytic stomata Subsidiaries monocyclic Subsidiaries dicyclic.

8 Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata because in a number of angiosperms taxa I have come across stomata in which some of the subsidiaries are arranged in a radiating fashion while others are otherwise (Figs.195,196, ). Further in a number of publications the stomata with radiating subsidiaries are also described as anomocytic stomata. For example, Fig. 10.3a represented by Wilkinson (1979) is more like an actinocytic stomata by definition but has designated as anomocytic stomata, and Fig.6a by Baranova (1987) is an anomocytic type but has been described as stephanocytic one. In order to avoid these confusions the present author prefer to categorise them as anomocytic stomata only and do not recognise actinocytic, stephanocytic stomata, etc. Cycles: Depending upon the cycles of subsidiaries the stoma may be described as monocyclic (Figs.53, 54, 63, 64), 1 1/2 cyclic ( hemidicyclic; Fig.77), dicyclic (Figs.55, 78 83), hemitricyclic (Figs.185), tricyclic and so on. However, the above definitions of stomata are not applicable to the abnormal stomata viz., stoma having more (Fig.87) or less than a pair of guard cells (Fig.88), abutting stoma (Figs.89, 90), etc. References: Anna M B, Prabhakar M. 1991a. Foliar architecture of some medicinal plants (Celastrales). Asian J Pl Sci, 3: Anna M B, Prabhakar M. 1991b. Foliar architecture in flora of Visakhapatnam. 1. Magnoliales. Indian J For, 14: Anna M B, Prabhakar M Foliar architecture of some medicinal plants of Visakhapatnam (Rubiales). Biome, 6(2): Anna M B, Prabhakar M. 1994a. Foliar architecture of some medicinal plants (Myrtales). Biol Sci Res Bull, 10:9 16. Anna M B, Prabhakar M. 1994b. Foliar architecture of some medicinal plants in Ficoidales. Chin J Bot, 6: Anna M B, Prabhakar M Foliar architecture of passiflorales occurring at Visakhapatnam. Geophytology, 24: Anna M B, Prabhakar M Foliar architecture of Asterales. Khan I A. Frontiers in Plant Science. Hyderabad, India: Anwarul Uloom Education Society Publ Anna M B, Prabhakar M, Ferzana J Foliar architecture of some medicinal plants (Verbenaceae). J Sci Res Pl Med, 13:8 16. Baranova M Historical development of the present classification of morphological types of stomata. Bot Rev, 53: Baranova M Principles of comparative stomatographic studies of flowering plants. Bot Rev, 58: Bhatia R Y P, Prabhakar M, Verma H K Forensic studies of poisonous and medicinal plants- Calatropis gigantia R. Br. (Asclepiadaceae). J Indian Acad For Sci, 25: Bhatia R Y P, Prabhakar M, Rao T S Dermotype studies on different cultivars of Beedi tobacco in relation to forensic science. J Indian Acad For Sci, 26:1 11. Cronquist A The evolution and classification of flowering plants. Steere W C, Glass H B. London: Thomos Nelson and Sons Ltd. Cutter G Plant Anatomy Part. London: Edward Arnold. Dilcher D L Approaches to the identification of angiosperm leaf remains. Bot Rev, 40: Eames A J, Mc Daniels L H An Introduction to Plant Anatomy. London: McGraw-Hill Book Co. Esau K Anatomy of Seed Plants. New Dehli, India: Wiley Eastern Ltd. Fahn A Plant Anatomy. New York: Pergamon Press. Ferzana J, Prabhaka M, Leelavathi P Foliar architecture in relation to taxonomy of Malvales. Asian J Pl Sci, 3(2): Ferzana J, Prabhakar M, Leelavathi P. 1994a. Structure, distribution and taxonomic significance of crystalliferous cells in Malvales. J Indian Bot Soc, 73: Ferzana J, Prabhakar M, Leelavathi P. 1994b. Pharmacognostic studies on foliar drugs (Malvaceae). J Sci Res Pl Med, 14,15: Florine R Untersuchungen Zur stammesgeschichte der coniferales and corditates. Svensk K Veternskaps Handl, 10(1): Florine R Studien Uber die cyacadales des mesozoikums. Svenska K Vetensk Akad Handl, 12:134. Francey P Etude de L appareil stomatique chez les, dictoyledones dans Un but taxinomique. Bull Soc Vaud Sci Nat, 59:1 12. Fryns-Claessens E, van Cotthem W A new classification of the ontogenetic types of stomata. Bot Rev, 39: Giesenhagen K Die Farngattung Niphobolus. Jena. Guyot Phylogenetic and systematic value of stomata in the umbillifereae. Heywood V H. The Biology and Chemistry of Umbelliferae. London: Academic Press Hortog R M, Bass P Epidermal characters of the Celastraceae sensu lato. Acta Bot Neerl, 27: Inamdar J A Epidermal structure and ontogeny of stomata in some Nyctaginaceae. Flora, 158: Inamdar J A Epidermal structure and development of stomata in some Polygonaceae. Proc Indian Acad Sci, LXX :

9 Inamdar J A, Mohan J S S, Subramanian R B Stomatal classification a review. Feddes Report, 97(3, 4): Jelani S, Leelavathi P, Prabhakar M Foliar epidermis in relation to taxonomy of Cleome (Capparaceae). Asian J Pl Sci, 2(2): Jelani S, Leelavathi P, Prabhakar M The morphological, anatomical, histochemical study of leaf Ocimum sanctum Linn (Lamiaceae). J Sci Res Pl Med, 12: Jelani S, Leelavathi P, Prabhakar M, Ferzana J Pharmacognostic studies on Centella asiatica (L.). Urban Ans Sci Life, 12: Jelani S, Prabhakar M Pharmacognostic studies of leaf of Hyptis suaveolens L. Ans Sci Life, 11(1, 2): Jelani S, Prabhakar M Pharmacognostic studies on leaf of Ocimum basilicum Benth (Lamiaceae). Biol Sci Res Bull, 8(1, 2): Jelani S, Prabhakar M Pharmacognostic study on leaf of Salvia officindalis L. J Sci Res Plants Med, 13: Kidwai P An illustrated glossary of technical terms used in stomatal studies. Dehra Dun, India: Bishen Singh Mahendra Pal Singh Publication. Koteshwar R K, Prabhakar M, Vijay kumar B K, Ramayya N Lithocysts and their taxonomic significance in Ficus L. subgenus Urostigma. Indian J Bot, 11: Leelavathi P, Prabhakar M, Ramayya N. 1984a. Structure, distribution, ontogeny and taxonomic significance of crystalliferous cells in Leguminosae. Indian J Bot, 7: Leelavathi P, Prabhakar M, Ramayya N. 1984b. Structure and ontogeny of Capitate hairs in Mimosa L. Geobios New Rep, 3 (2): Leelavathi P, Prabhakar M, Ramayya N Cavitated trichomes in Caesalpinioideae (Leguminosae). Iselya, 2: Leelavathi P, Prabhakar M, Ramayya N. 1988a. Pharmacognostic studies on the leaf of Acalypha indica L. Indian J Bot, 11: Leelavathi P, Ramayya N Rapid isolation of leaf epidermis by double-treatment method. Geobios, 2: Leelavathi P, Ramayya N, Prabhakar M Foliar stomatal distribution patterns in the Leguminosae and their taxonomic significance. Phytomorphology, 30 (2, 3): Leelavathi P, Ramayya N, Prabhakar M Study of the leaf costal cell distribution patterns and their taxonomic significance in Legumionosae. Geophytology, 11: Leelavathi P, Veerabhadra Rao A, Prabhakar M, Vijay Kumar B K. 1988b. Structure, distribution and ontogeny of cylindrical hair in Leguminsoae. J Swamy Bot Cl, 5(1): Maroti I Untersuchung der Epidermis von Pteropsida- Blatt mit besonderer Rucksicht auf die einheimischen Arten. Acta Biol (Szeged), (3, 4): Maroti I Untersuching der Entwicklung der Epidermis des Psilotinae und des Filicinae-Blattes und der Entwicklung der Stomas. Acta Biol (Szeged), (3, 4): McLean R C, Cook W R I Text Book of Theoritical Botany Vol. 1. N. York, London: University of Toronto Press. Metcalfe C R The anatomical approach to systematics: general introduction with special reference to recent work on monocatyledons. Rec Adv Bot, 1: Metcalfe C R, Chalk L Anatomy of Dicotyledons, Vols. and. Oxford: Clarendon Press. Mickel J T A monographic study of the fern genus Anemia, subgenus Captophyllum. Iow State J Sci, 36: Mickel J T, Lersten N R Floating stomates (adetostomy) in ferns: distribution and ontogeny. Am J Bot, 54: Padma R P, Prabhakar M, Ramayya N Trichome distributional patterns and their taxonomic significance in Clerodendrum L. J Swamy Bot Cl, 5(2): Paliwal G S The development of stomata in Linum usitatissium L. Curr Sci, 30: Paliwal G S. 1969a. Stomata in Certain Angiosperms: their Structure, Ontogeny and Systematic Value, in Recent Advances in Anatomy of Tropical Seed Plants. Delhi: Hindustan Publication. Paliwal G S. 1969b. Stomatal ontogeny and phylogeny.. Monocotyledons. Acta Bot Neerl, 18: Pant D D On the ontogeny of stomata and their homologous structure. Plant Sci Series :1 24. Patel J D How should we interpret and distinguish subsidiary cells? Bot J Linn Soc, 77: Patel J D New morphological classification of stomatal complexes. Phytomorphology, 29: Payne W W Helicocytic and allelocytic stomata: unrecognized patterns in the dicotyledonae. Am J Bot, 57: Payne W W Stomatal patterns in embryophytes: their evolution ontogeny and interpretation. Taxon, 28: Prabhakar M, Anna M B Foliar architecture of sapindales occurring at Visakhapatnam. J India Bot Soc, 74:9 14. Prabhakar M, Anna M B Foliar architecture in identification of the flora. Khan I A. Frontiers in Plant Science. Hyderabad, India: Anwarul Uloom Education Society Publ.

10 Malvey PRABHAKAR: Structure, Delimitation, Nomenclature and Classification of Stomata Prabhakar M, Bhatia R Y P, Verma H K. 1988a. Forensic studies of poisonous and medicinal plants Casacabela thevetia (L.). Lippold (Apocynaceae). Indian J For Sci, 2: Prabhakar M, Leelavathi P Structure, delimitation, nomenclature and classification of plant trichomes. Asian J Pl Sci, 1 (1): Prabhakar M, Leelavathi P Structure and ontogeny of unicellular conical hairs in Leguminosae. J Swamy Bot Cl, 8(1, 2): Prabhakar M, Leelavathi P Structure, delimitation and distribution of paracytic stomata in Leguminasae and Portulacaceae. J Swamy Bot Cl, 9 (3, 4): Prabhakar M, Leelavathi P, Ramayya N Structure, distribution and ontogeny of multiseriate conical hairs in Leguminosae. Proc Nat Acad Sci, 56: Prabhakar M, Leelavathi P, Jelani S, Shoba Rani G, Narayan R Pharmacognostic studies of Adatoda zeylanica medicus. J Swamy Bot Club, 7(1, 2):1 7. Prabhakar M, Ramayya N Structure and development of trichomes in the family Portulacaceae. Mohan Ram H Y, Shah J J, Shah C K. Form Structure and Function in Plants. Johri B M. Commemoration Volume. Sarita Prakashan, Nauchandi, Meerut, India Prabhakar M, Ramayya N Anatomical studies in the Indian Portulacaceae.. Leaf Lamina, Histochemistry, Developmental and Structural Anatomy of Angiosperms. Pereasamy K. Symposium Volume. Tiruchirapally, India: P and B Publications Prabhakar M, Ramayya N, Leelavathi P Structure and distribution of epidermal elements in the angiosperms.. Epidermal cell complex. Geophytology, 14: Prabhakar M, Rao T S, Bhatia R Y P. 1988a. Micromorphological studies on tobacco and its significance in forensic science. Indian J For Sci, 2: Prabhakar M, Shoba R G, Narayan R, Leelavathi P. 1988b. Structure distribution and taxonomic significance of lithocysts and cystoliths in Acanthaceae. J Swamy Bot Cl, 5: Prabhakar M, Vijay K B K, Ramayya N, Leelavathi P Structure, distribution and taxonomic significance of trichomes in some Indigofera L. (Fabaceae). Proc Indian Acad Sci (Plant Sci), 95: Prantle K Die Ergebnisse der neueren untersuchugen Uberdie spaltoffnungen. Flora, 55: , , , Prantle K Untersuchungen zur Morphologie der Gefasskryptogamen.. Die Schizaeaceen. Leipzig W. Engelman. Prat H Vers une classification naturelle des Graminees. Bull Soc Bot France, 107(1, 2):51. Probst W Vergleichende morphologie und Entwicklungs geschiete der spltaffnungen bei Farnen. Dissertation University Tubingen. Rajagopal T Flora of Hyderabad including a study of the foliar epidermal characters of the species as an aid to taxonomy. PhD Thesis, Hyderabad: Osmania University. Ramayya N, Leelavathi P, Prabhakar M Pharmacognostic studies in the leaf of Tylophora indica (Burm.f.). Merr Hahne, Glean, 50: Ramayya N, Prabhakar M Growth dynamics and developmental patterns in the unicellular trichomes of angiosperms. Curr Sci, 42: Ramayya N, Prabhakar M Morphology of the shaggy appendages. Elatinaceace. J Indian Bot Soc, 54: Rao T S, Prabhakar M, Bhatia R Y P, Verma H K Dermotype studies of beedi wrappers of different brands and its significance to forensic science. Indian J For Sci, 5: Rao T S, Bhatia R Y P, Prabhakar M. 1992a. Morphochemical analysis of beedies in relation to forensic science. J Indian Acad For Sci, 31: Rao T S, Prabhakar M, Bhatia R Y P. 1992b. Epidermal studies on different brands of beedies as an aid to criminal investigation. Indian J For Sci, 6: Rao T S, Prabhakar M, Bhatia R Y P. 1992c. Epidermal studies on cigarette tobacco cultivars in relation to forensic science Indan. J Criminol Criminoastics, 13(3, 4): Rao T S, Bhatia R Y P, Prabhakar M, Verma H K. 1993a. Micromorphological studies on different brands of beedi wrappers and its significance to forensic science. Adva Pl Sci, 6: Rao T S, Jelani S, Bhatiya R Y P, Prabhakar M. 1993b. Foliar surface characters of Nicotiana tabacum L. cultivars in relation to forensic science. J Indian Bot Soc, 74: Rao T S, Prabhakar M, Bhatia R Y. 1993c. Dermotype studies on different brands of cigarettes as an aid to criminal investigation Adl. Tip Derg, 9: Rasmussen H Terminology and classification of stomata and stomatal development. Bot J Linn Soc, 83: Shtromberg A Y A On the question of classification of stomatal types of dicotyledonous plants. Sci Publ Chem Pharmoc Inst, 8:51 66.

11 Simola L K Comparative studies on number of leaflets, venation and epidermal structure in the genus Lathyrus. Can J Bot, 46: Solereder H Systematic Anatomy of the Dicotyledons. Vol. 2. Oxford: Clarendon Press. Stace C A Cuticular studies as an aid to plant taxonomy. Bull Brit Muss Bot, 4:1 78. Stevens R A, Martin E S A new ontogenetic classification of stomatal types. Bot J Linn Soc, 77: Tomlinson P B Development of stomatal complex as a taxonomic character in the Monocotyledons. Taxon, 23: van Cotthem W. 1970a. Comparative morphological study of the stomata in the Filicopsida. Bull Jard Bot Nat Belg, 40: van Cotthem W. 1970b. A classification of stomatal types. Bot J Linn Soc, 63: Verma H K, Bhatia R Y P, Prabhakar M, Rao T S Forensic studies of poisonous and medicinal plants- Abrus precatorius L. (Fabaceae). Front For, 1: Verma H K, Bhatia R Y P, Prabhakar M Forensic studies of poisonous and medicinal plants IV. Nerium indicum Miller (Apocynaceae). J Indian Acad For Sci, 30: Verma H K, Bhatia R Y P, Prabhakar M, Rao T S Forensic studies of poisonous and medicinal plants. Argemone mexicana L. (papavaraceae). Indian J For Sci, 6: Vesque J De l emploi des caracteres anatomiques dans la classification des vegetaux. Bull Soc Bot Fr, 36: Vijay Kumar B K, Prabhakar M, Ramayya N, Leelavathi P Structure, distribution and development of cavitated trichomes in Indigofera L. (Fabaceae). Geophytology, 16: Wilkinson H P The plant surface (Mainly leaf) part 1: stomata in the anatomy of the dicotyledons. Vol. 1. Metcalfe C R, Chalk L. 2nd ed. Oxford: Clarendon Press (Managing editor: HE Ping)

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