P-type sieve-element plastids and the systematics of theArales (sensuCronquist 1988)—with S-type plastids inPistia

The sieve-element plastids of 126 species of theArales were investigated by transmission electron microscopy. With the exception ofPistia (with S-type plastids) all contained the monocotyledon specific subtype-P2 plastids characterized by cuneate protein crystals. While the species studied from bothAcoraceae andLemnaceae have form-P2c plastids (i.e., with cuneate crystals only), those of theAraceae belong to either form P2c (14 species), P2cs (the great majority) or P2cfs (Monstera deliciosa, only, with form-P2cs plastids in the otherMonstera species studied). The form-P2cs plastids of theAraceae are grouped into different categories according to the quantity and quality of their protein and starch contents. The subfamilyLasioideae is redefined to comprise all aroid P2c-taxa and those P2cs-genera that contain only one or very few starch grains. Only little starch is also recorded in the sieve-element plastids ofGymnostachys (Gymnostachydoideae), with the other plastid data denying a close relationship toAcorus. While equal amounts of starch and protein are generally present in sieve-element plastids of the subfamiliesPothoideae, Monsteroideae, Colocasioideae, Philodendroideae, andAroideae, maximum starch content and only very few protein crystals are found in form-P2cs plastids ofCalla (Calloideae),Ariopsis (Aroideae), andRemusatia (Colocasioideae?). In the latter, both morphology and size of sieve-element plastids are close to those ofPistia.—In theAraceae the diameters of the sieve-element plastids exhibit a great size range, but are consistent within a species and within a defined part of the plant body. Comparative data are mainly available for stem and petiole sieve-element plastids.—The accumulated data are used to suggest an affiliation of the species to subfamilies and to discuss the phylogeny of theArales. Forms and sizes of their plastids support a separation of bothAcoraceae andLemnaceae from theAraceae. The presence of S-type plastids inPistia does not favour direct and close relationships to the form-P2c genusLemna.—The prevailing form-P2cs plastids might support proposals that place theArales (together with also form-P2cs plastid containingDioscoreales) in the neighbourhood of basal dicotyledons. BesidesAsarum andSaruma (Aristolochiaceae), with monocotyledonous form-P2c plastids,Pistia (with dicotyledonous S-type plastids) gives another example for a link between the two angiosperm classes.     

Contributions to the knowledge of sieve-element plastids inGunneraceae and allied families

P-type sieve-element plastids were found in theGunneraceae, while S-type plastids are present in theHaloragaceae andHippuridaceae. The specific characters of the sieve-element plastids (e.g., their size and the morphology of their contents) are discussed in relation to other taxa of theRosidae containing P-type plastids and to the systematic position of theGunneraceae. Contributions to the Knowledge of P-Type Sieve-Element Plastids in Dicotyledons, III. — For other parts of this series see (I.:)Behnke (1982 b) and (II.:)Behnke (1985).     

Starch-accumulating (S-type) sieve-element plastids in Hydatellaceae: implications for plastid evolution in flowering plants

TEM investigation of sieve-element plastids in three species of Trithuria, the sole genus of the small aquatic family Hydatellaceae, show that P-type plastids are absent from this genus and only starch-accumulating (S-type) sieve-element plastids are present. This discovery is consistent with the recent transfer of Hydatellaceae from the highly derived monocot order Poales (grasses and their allies) to the early-divergent angiosperm order Nymphaeales (waterlilies) based on molecular phylogenetic data. Species of Poales consistently possess P2-subtype plastids, in common with other monocots, but only S-type plastids are present in Nymphaeales. The results confirm that Hydatellaceae do not belong in monocots. Optimisation of the two major types of sieve-element plastid onto a recent phylogeny of early-divergent angiosperms confirms that S-type is the primitive form and indicates that P-type sieve-element plastids have evolved more than once in angiosperms.     

Ultrastructure of sieve-element plastids inCaryophyllales (Centrospermae), evidence for the delimitation and classification of the order

The orderCaryophyllales (Centrospermae) was found to contain specific P-type sieve-element plastids which are characterized by protein inclusions composed of ring-shaped bundles of filaments and of central crystalloids. The sieve-element plastids of 14 families (140 species investigated) fit into this overall characterization, and more specific details are used to delimit the families and arrange them within the order.Phytolaccaceae, the basic family of the order display much diversity: the crystalloids inside their plastids are either globular (most genera) or polygonal (Stegnosperma), starch may also be present (Phytolacca).Nyctaginaceae, with starch inBougainvillea sieve-element plastids, can be derived directly fromPhytolacca. Globular crystalloids are present in most of the families, as inDidiereaceae, Cactaceae, Aizoaceae-Tetragoniaceae, Portulacaceae-Basellaceae-Halophytaceae-Hectorellaceae. Caryophyllaceae andLimeum ofMolluginaceae contain polygonal crystalloids (otherMolluginaceae with globular crystalloids). Crystalloids are entirely absent fromChenopodiaceae (incl.Dysphaniaceae) andAmaranthaceae. The probable relationships between these families are presented diagrammatically in Fig. 13. Bataceae, Gyrostemonaceae, Vivianiaceae, Theligonaceae, Polygonaceae, Plumbaginaceae, Fouquieriaceae, Frankeniaceae, andRhabdodendraceae—all at some time included into theCaryophyllales (Centrospermae) or doubtfully referred to them—develop S-type (or different P-type) sieve-element plastids. Their direct connection to theCaryophyllales therefore is excluded. Finally, evolutionary trends of theCaryophyllales are discussed.Presented in the Symposium Evolution of Centrospermous Families, during the XIIth International Botanical Congress, Leningrad, July 8, 1975.     

Further studies of the sieve-element plastids of theCaryophyllales includingBarbeuia,Corrigiola, Lyallia,Microtea, Sarcobatus,andTelephium

The sieve-element plastids of 69 species of theCaryophyllales were investigated by transmission electron microscopy. All contained the specific subtype-P3 plastids characterized by a peripheral ring of protein filaments. The presence or absence of an additional central protein crystal and their shape being either polygonal or globular as well as the average sizes of the sieve-element plastids are useful features in the characterization of some families.—Barbeuia contains sieve-element plastids that confirm its placement within thePhytolaccaceae. Lyallia differs fromHectorella by including small starch grains in their sieve-element plastids, which otherwise by their globular crystals negate a closer connection to theCaryophyllaceae. The lack of a central protein crystal in its form-P3fs plastids placesMicrotea best within theChenopodiaceae. Sarcobatus, a so far uncontested member of theChenopodiaceae, contains form-P3cf plastids, i.e., including a central crystal not found elsewhere in this family.Telephium andCorrigiola, shifted back and forth betweenMolluginaceae andCaryophyllaceae, have form-P3cf(s) plastids with a polygonal crystal which favor their placement within theCaryophyllaceae.     

Sieve-element characters of Myristicaceae: Nuclear crystals, S-and P-type plastids, nacreous walls

The phloem of the Myristicaceae is composed of sieve elements, parenchymatous cells, and fibers. Within the metaphloem and secondary phloem parenchymatic layers including prominent secretory elements alternate with tangential bands of fibers and layers composed of sieve elements, companion cells and phloem-parenchyma cells. among the latter the sieve elements are most abundant and easily identified by the presence of thick (nacreous) walls. The most characteristic feature of the sieve elements of Myristicaceae (and found nowhere else among the Magnoliiflorae) are nuclear crystals, which are released into the lumen during nuclear degeneration and persist in the mature cell. P-and S-type sieve-element plastids were recorded for the 18 species investigated. Both types of the plastid are characterized by large diameters and many medium-sized starch grains. The sizes and contents (small protein crystals only) of the P-type plastids of the Myristicaceae do not conform to the tiny P-type plastids (with large protein crystals) of the Annonaceae, a family to which the Myristicaceae is traditionally allied.     

Ultrastructural,micromorphological and phytochemical evidence for a “Central Position” ofMacarthuria (Molluginaceae) within theCaryophyllales

Subtype PIII sieve-element plastids, anthocyanins, spinulose, perforate-tectate pollen grains and the specific seed-coat sculpturing found in twoMacarthuria species (M. australis, M. neocambrica) consolidate their placement withinMolluginaceae. The unique form of the sieve-element plastids, i.e. with cubic crystals and starch grains (PIIIc″fs), finds its closest counter-part inLimeum. The multiple intertwinement of different genera of theMolluginaceae with many other centrospermous families led to a consideration of their more central position withinCaryophyllales.     

Sieve-element plastids,exine sculpturing and the systematic affinities of theBuxaceae

The sieve-element plastids of members of several genera in theBuxaceae (Buxus, Pachysandra andSarcococca) were found to be of the specific subtype PVI, which contains a central globular protein crystal.Simmondsia (Simmondsiaceae) andDaphniphyllum (Daphniphyllaceae), on the other hand, were found to contain S-type sieve-element plastids. The occurrence of the highly restricted PVI plastids in theBuxaceae mitigates against a close relationship between theBuxaceae andSimmondsia, Daphniphyllum andEuphorbiaceae. Exine sculpturing of theBuxaceae andSimmondsiaceae also shows no close similarities. Both of these EM characters are discussed in connection with other available data and with respect to earlier systematic treatment of these families.     

P-type sieve-element plastids present in members of the tribesTriplareae andCoccolobeae (Polygonaceae) renew the links between thePolygonales and theCaryophyllales

Form-Pfs sieve-element plastids were found inTriplaris, Ruprechtia, andCoccoloba (Polygonaceae) while other genera of the family and those studied from the often associatedPlumbaginaceae contain S-type sieve-element plastids. The rareness of form-Pfs plastids among the angiosperms, their similarity to the peculiar form-P3fs plastids of theChenopodiineae, and the comparatively small plastid diameters measured for all forms present in theCaryophyllales, Polygonales, andPlumbaginales suggest close relationships between these taxa. The restriction inPolygonaceae of form-Pfs plastids to the closely allied tribesTriplareae andCoccolobeae is discussed with regard to both the intrafamilial and ordinal phylogeny, and also considering possible connections to the only magnoliidaean Pfs-taxonCanella. Dedicated to Univ.-Prof. DrF. Ehrendorfer on the occasion of his 70th birthday.     

Sieve-element plastids ofCyrillaceae,Erythroxylaceae andRhizophoraceae: Description and significance of subtype PV plastids

A new subtype (PV) of protein-containing sieve-element plastids was found to contain a uniquely large number of polygonal protein crystals, sometimes with (PVcf) and sometimes without (PVc) protein filaments. These plastids do not accumulate starch. The PVcf-plastids occur inCyrillaceae only, while the PVc-plastids are limited toErythroxylaceae andRhizophoraceae. The significance of the new P-subtype with respect to the systematic position of the three families is discussed.     

Elektronenmikroskopische Untersuchungen zur Frage der verwandtschaftlichen Beziehungen zwischenTheligonum undRubiaceae: Feinbau der Siebelement-Plastiden und Anmerkungen zur Struktur der Pollenexine

Theligonum cynocrambe and 13 species ofRubiaceae contain S-type sieve-element plastids, wide-spread in Dicotyledons. Alignment ofTheligonum toCaryophyllales (Centrospermae), especiallyPhytolaccaceae, is unlikely, because this order is characterized by specific P-type plastids. SEM investigations show the pollen exine ofTheligonum to be microreticulate, with additional supratectate spinules.Asperula and other genera of the tribeRubieae have a tectum perforatum (punctitegillate sexine), also with supratectate verrucae or spinulae.—Thus ultrastructure suggests (but not definitely proves) relationships betweenTheligonum andRubiaceae, while affinities betweenTheligonum andCaryophyllales are excluded.

     

Form-Pfs Plastids,Stem Anatomy and Systematic Affinities of Stylobasium Desf. (Stylobasiaceae)

The vascular system of the stem of Stylobasium was investigated during its primary and secondary phases with both light and electron microscopic methods. It contains collateral bundles arranged in a ring, separated by rays which undergo regular cambial growth. The phloem consists of short sieve elements connected to sieve tubes by simple sieve plates, companion cells of the same length, and phloem parenchyma cells. During their autophagy-like differentiation and maturation, typical of all angiosperms, the sieve elements of Stylobasium have a peculiar feature, whereby they develop and retain form-Pfs plastids (containing protein filaments and starch). The sieve-element plastids of the two Stylobasium species, and of some 100 species belonging to taxa of which Stylobasium had been considered to be a possible member, have been studied by transmission electron microscopy. With the exception of a few species with form-Pcs plastids (containing a single small protein crystal in addition to starch), the great majority of taxa studied are characterized by S-type sieve-element plastids (containing starch only). The presence of form-Pfs plastids in Stylobasium supports its separation into the unigeneric Stylobasiaceae and the placement of this family close to other form-Pfs or form-Pcfs-containing taxa. While other characters would exclude an affiliation to the Magnolianae (form-Pfs plastids in Canella) or Caryophyllales (form-Pfs plastids in Microtea), an association with the form-Pcfs families Connaraceae and Mimosaceae is positively considered and corresponds to their frequent allocation close to the Rutales and Sapindales. Within the Rutales/Sapindales the sizes of sieve-element plastids (average diameter) range from very large (e.g. in the Julianaceae) to comparatively small (e.g. in Aceraceae) and are used to group the families. The sieve element characters of the Coriariaceae (tiny plastids with almost no starch, wide sieve plate pores, copious P-protein) suggest their removal from Rutales/Sapindales into the neighbourhood of the Cucurbitaceae.     

S-type sieve-element plastids and anthocyanins inVivianiaceae: Evidence against its inclusion intoCentrospermae

The presence of S-type sieve-element plastids and anthocyanins in theVivianiaceae indicates that it is not a member ofCentrospermae (Caryophyllales).     

The development of specific sieve-element plastids in wound phloem ofColeus blumei (S-type) andPisum sativum (P-type), regenerated from amyloplast-containing parenchyma cells

Protoplasma - In experimentally-induced wound phloem, sieve-element plastids express their genetically determined type in depositing amylopectinrich sieve-tube starch (Coleus, S-type) and polygonal...     

Sieve-Element Plastids,Nuclear Crystals and Phloem Proteins in the Zingiberales

The sieve-element characters of 40 species from all families making up the monocotyledon order Zingiberales have been studied by transmission electron microscopy. While phloem-proteins are a typical component of all eight families, the Zingiberaceae are characterized by nondispersive protein bodies derived from nuclear crystals. The sieve-element plastids are of the form-P2cs, i.e. contain cuneate protein crystals (as typical of all monocotyledons) and starch grains, those of the family Musaceae have protein filaments in addition (form-P2cfs). The exclusiveness of the form-P2c(f)s plastids contributed to the homogeneity of the order and its distinctness among other monocotyledon taxa. When diameters of the sieve-element plastids from leaf phloem are compared, in the “banana group” the family averages of the Strelitziaceae and the Lowiaceae have, respectively, maximum and minimum values and are clearly different from those in the Musaceae, the family in which they have been included previously. In the “ginger group”, the family averages of the Zingiberaceae, Costaceae, and Marantaceae are close to the order average, with only Cannaceae having minimum values. A comparison of species averages, however, reduces the size differences between families: the value for Ravenala (Strelitziaceae) is close to those of the five Musaceae tested, and that of Globba (Zingiberaceae) even slightly lower than the species average of Canna.     

Sieve-element plastids and evolution of monocotyledons, with emphasis on Melanthiaceae sensu lato and Aristolochiaceae-Asaroideae, a putative dicotyledon sister group

Monocotyledons are distinguishable from dicotyledons by their subtype P2 sieve-element plastids containing cuneate protein crystals, a synapomorphic character uniformly present from basal groups through Lilioids to Commelinoids. The dicotyledon generaAsarum andSaruma (Aristolochiaceae-Asaroideae) are the only other taxa with cuneate crystals, but their sieveelement plastids include an additional large polygonal crystal, as is typical of many eumagnoliids. New investigations in Melanthiaceae s.l. revealed the same pattern (polygonal plus cuneate crystals) in the sieve-element plastids ofJaponolirion osense (Japonoliriaceae/Petrosaviaceae), ofHarperocallis flava, Pleea tenuifolia, andTofleldia (all: Tofieldiaceae). InNarthecium ossifragum a large crystal, present in addition to cuneate ones, usually breaks up into several small crystals, whereas inAletris glabra andLophiola americana (Nartheciaceae) and in all of the 15 species studied and belonging to Melanthiaceae s.str. only cuneate crystals are found. Highresolution TEM pictures reveal a crystal substructure that is densely packed in both cuneate and polygonal forms, but in Tofieldiaceae the polygonal crystals stain less densely, probably as a result of the slightly wider spacing of their subunits. The small crystals ofNarthecium are “loose”; that is, much more widely spaced. Such “loose” crystals are commonly found in sieve-element plastids of Velloziaceae, present there in addition to angular crystals, and together with cuneate crystals in a few Lilioids and many taxa of Poales (Commelinoids). Ontogenetic studies of the sieve elements ofSaruma, Aristolochia, and several monocotyledons have shown that in their plastids cuneate crystals develop very early and independent from a polygonal one present in some taxa. Therefore, a conceivable particulation of polygonal into cuneate crystals is excluded. Consequently, mutations of some monocotyledons that contain a lone, large, polygonal crystal in their sieve-element plastids are explained as the result of a complex genetic block. The total result of all studies in sieve-element plastids suggests thatJaponolirion and Tofieldiaceae are the most basal monocotyledons and that Aristolochiaceae are their dicotyledon sister group.     

Theligonaceae: Pigment and ultrastructural evidence which excludes it from the order centrospermae

The discovery of anthocyanins (and no betalains) along with S-type sieve-element plastids in Theligonum cynocrambe supports the exclusion of this taxon from the order Centrospermae.     

Sieve-Element Characters of the Proteaceae and Elaeagnaceae: Nuclear Crystals,Phloem Proteins and Sieve-Element Plastids

The sieve-element characters of 34 species from the Proteaceae and Elaeagnaceae have been studied by transmission electron microscopy. While nondispersive protein bodies and dispersive P-protein are typical components of both families, specific forms and/or their distinctive origin accentuate some taxa. Within the Grevilloideae, subfamily of Proteaceae, a number of Australian species and genera contain protein crystals of nuclear origin arranged into rosette-like bodies, while in the other members studied from the same subfamily no nondispersive protein bodies were found. Several Australian and South African genera of the Proteoideae contain compound-spherical nondispersive protein bodies that reside in the cytoplasm from their very beginning. In the Elaeagnaceae three different P-protein bodies are present of which one is tubular and dispersing, another is nondispersive and of irregular-stellate form, and a third is globular (resembling a P-protein from Cucurbita). The great majority of the species studied from the Proteaceae contains form-Ss sieve-element plastids, Lomatia ilicifolia and Macadamia ternifolia are distinct in having form-Pcs plastids. The average diameter of stem sieve-element plastids in the family is 1.38 μm. The Elaeagnaceae (three species investigated) is a pure form-So family (average diameter: 0.8 μm). There are no specific sieve-element characters that would support any relationship between the Proteaceae and Elaeagnaceae. While affinities of the former to pre-Gondwanan parts of the Rosanae/Myrtanae are discussed, a reconsideration of the Elaeagnaceae as a possible member of the Violanae (identical features with Cucurbitaceae) is proposed.     

THE LATERAL MERISTEM AND ITS DERIVATIVES IN THE CORM OF ISOETES MURICATA

Corm tissue of Isoetes muricata Dur. was fixed in glutaraldehyde and postfixed in osmium tetroxide for electron microscopy. Very young secondary sieve elements can be distinguished from contiguous cambial cells by their distinctive plastids and by the presence of crystalline and/or fibrillar proteinaceous material in dilated cisternae of rough endoplasmic reticulum (ER). At maturity, the sieve elements are lined by the plasmalemma and a parietal, anastomosing network of smooth ER. Degenerate nuclei persist in all mature sieve elements. In addition, mature sieve elments contain plastids and mitochondria. Sieve-area pores are present in all walls. The lateral meristem of I. muricata consists of 2–3 layers of cells year-round. Judging from numerous collections made between October 1972 and July 1975, new sieve-element differentiation precedes cambial activity by about a month. Early in May, 1–2 cells immediately adjacent to already mature sieve elements differentiate directly into sieve elements without prior division. In early June, at about the time sieve-element differentiation is completed, cambial division begins. Division is sporadic, not uniform throughout the meristem. Dormancy callose accumulates in the secondary sieve elements in late October, and is removed in early May, at about the same time new sieve-element differentiation begins. Cells of the dormant cambium are characterized by the presence of numerous small vacuoles and large quantities of storage materials, including lipid droplets, starch grains, and tannin. By contrast, active cambial cells contain few large vacuoles with little or no tannin, and they have little storage material.     

Zum Feinbau der Siebröhren-Plastiden von Aristolochia und Asarum (Aristolochiaceae)

Summary Sieve-tube plastids of Aristolochia (5 species investigated) contain several starch grains and always one large crystalloid. In Asarum (3 species investigated) starch has not been found in the sieve-tubes. Their plastids contain several cuneate crystalloids that are sometimes arranged around an invisible centre. Asarum sieve-tube plastids look almost like typical plastids of monocotyledon sieve-tubes.-Crystalloids of Aristolochia and of Asarum sieve-tube plastids are composed of 50–60 Å subunits in straight and parallel order as crystalloids in monocotyledon sieve-tube plastids are.The results of the investigations of the fine structure are discussed in relation to the position of the Aristolochiaceae in the system of angiosperms.