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Home , Aphyllanthes, Aristea, Astelia banksii, Beaucarnea, Beaucarnea recurvata, Calibanus

lAWA Journal, Vol. 16 (3),1995: 261-268

NEW RECORDS OF SECONDARY THICKENING IN by Paula Rudall Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, United Kingdom

SUMMARY

A secondary thickening is recorded for the first time in some herbaceous taxa of (Herreria montevidensis and Thysanotus spiniger), and the new records are assessed in a systematic context. Key words: Secondary thickening meristem, monocotyledons, Aspara• gales.

INTRODUCTION

All monocotyledons lack a vascular cambium, which is typically a single persistent row of cells producing phloem centrifugally and xylem centripetally. However, some monocotyledons achieve stem thickening by means of a different type of lateral meristem, either a primary thickening meristem (PTM) near the apex, together with diffuse (as in palms), or a secondary thickening meristem (STM) further away from the apex (as in some Asparagales; see Rudalll991, for review). The PTM and STM are probably developmentally related, although there is complex tissue involvement. In taxa with an STM, the PTM and STM may sometimes be longitudi• nally continuous, at least at some stage in the life cycle (Stevenson 1980). Virtually all monocotyledons have a PTM, but among -forming or woody taxa this has developed along different lines, probably more than once, either as an exten• sive apical PTM, as in palms, or as an STM, in some Asparagales (see below). The PTM and STM are not homologous with the vascular cambium, as they are tiered (etagen) which produce distinct vascular bundles (of both xylem and phloem) in a parenchymatous ground tissue (Fig. 1-3), mainly centripetally. There are records of a PTM in some and other groups (DeMason 1983), although the homology of these requires testing. All unequivocal records of an STM are in the asparagoid clade (sensu Chase et al. 1995), which comprises Dahlgren et al.'s (1985) order Asparagales, together with a few members of their Liliales, such as (RudallI991). A STM has been re• ported in several tree-forming and shrubby asparagoids: Agave, Aloe, , Calibanus, , , , Furcraea, Klattia, Nivenia, , Pleomele, , Witsenia, and , and also in some more her• baceous taxa with a thick 'woody' or stem, such as , Gasteria,

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Fig. 1-3. Cordyline rubra, stem cross sections in region of secondary thickening meristem (m). Secondary vascular bundles = sv. - Scale bars = 100 iJl1l.

Haworthia, Lomandra, Patersonia and (Table 1). However, many herba• ceous taxa have not hitherto been examined for this character, due to problems of obtaining material, particularly of underground organs. This paper records new examples of taxa with an STM and assesses them in a sys• tematic context, as part of an ongoing systematic survey of Asparagales.

MATERIAL AND METHODS

Material examined was from the living collections of the Royal Botanic Gardens, Kew (HK) and field-fixed material collected by the author in (PERTH). Material

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Fig. 4-6. Cross sections of woody underground , showing secondary thickening meristem (s), radially aligned secondary vascular bundles (sv) and central primary vascular bun• dles (pv). - 4: Lomandrafiliformis. - 5 & 6: Herreria montevidensis. - Scale bars = 100 j.lIll.

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Fig. 7-9. Cross sections in region of lateral meristems. - 7: Thysanotus spiniger, woody under• ground rhizome, with STM (s) and secondary vascular bundles (sv) in an extensive paren• chymatous (radially aligned) ground tissue. - 8 & 9: Chlorophytum suffruticosum, pachycaul above-ground stem, with lateral meristem (m) and few derivative vascular strands. - Scale bars = JOO J.IIIl.

was selected from asparagoid taxa unknown for this character, with a thick under• ground rhizome: banksii A. Cunn. (HK 1986-3620); A. grandis Hook. f. ex Kirk (HKI972-3488); Chlorophytum suffruticosum Baker (HKI973-1912); W. Hill ex Benth. (HKI984-5398); Herreria montevidensis Klotzsch ex Griseb. (HKI977-68); Hemiphylacus latiJolius S. Watson (HKI979-3739); Hypoxis urceolata Nel. (HK1975-260); Lomandra preissii (Endl.) Ewert (PERTH: P. 1. Rudall 19), L..fili• formis (Thunb.) Brittan (Morrison 1486); Thysanotus spiniger Brittan (PERTH: P. J. Ruda1145); callistemon W. R. B. 01iv. (HK1974-1783). Living material was fixed in formalin acetic alcohol (FAA) and stored in 70% ethanol. Dried herbarium material was revived by boiling in water. Sections were cut using a Reichert sliding microtome, stained in safranin and Alcian blue, dehydrated through an alcohol series to 100% ethanol then Histoclear, mounted onto microscope slides in Euparal, and examined using normal bright-field optics on a Leitz Diaplan photo• microscope.

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RESULTS

Of the taxa examined here, a persistent pericyclic meristem (PTM / STM) is present at some distance (several centimetres) from the apex in Herreria, Lomandra, Thysanotus and Chlorophytum, but not in the other genera investigated (Astelia, Doryanthes, Hemi• phylacus, Hypoxis, Xeronema), where the PTM is restricted to the apical region and does not produce extensive derivatives. In Herreria montevidensis (Fig. 5, 6) and Lomandra spp. (Fig. 4) there is a 'typical' STM (i. e. as in Dracaena or Cordyline, Fig. 1-3), with derivatives of radially aligned chains of vascular bundles in a parenchymatous ground tissue, resulting in a 'woody' underground stem. In Thysanotus spiniger (Fig. 7) the radially-aligned centripetal derivatives are ex• tensive, indicating that the lateral meristem is an STM. However, the derivatives are more parenchymatous than in more 'typical' examples (e.g. Herreria and Lomandra), with sparse radially-aligned bundles in a ground tissue of initially parenchymatous cells, which often become lignified, resulting in a 'woody' underground stem. In Chlorophytum suffruticosum (Fig. 8, 9) a pericyclic (lateral) meristem is present several (20 or more) cm from the apex, resulting in a tall, evenly thick (pachycaul) aerial stem. However, although too far from the apex to be a 'normal' PTM, this meri• stem cannot be regarded as a typical STM, as its derivatives are relatively sparse and largely parenchymatous (with some small vascular bundles: Fig. 9).

DISCUSSION

The new records listed here supplement the number of genera recorded as including with an STM (Table 1). However, the exact definition of an STM is problem• atical. In arborescent taxa such as Agave, Cordyline and Dracaena, and in some herba• ceous taxa such as Aphyllanthes, Herreria, Lomandra and Patersonia, the presence of an STM is unequivocal, but there are also transitional taxa. There is a clear relation• ship between the STM and the PTM, the latter being almost ubiquitous in monocots. A relatively extensive PTM, extending many internodes from the apex (rather than form• ing extensive derivatives close to the apex, as in palms), is widespread amongst Asparagales (RudallI991), but rare elsewhere in monocotyledons (except e. g. Veratrum: Cheadle 1937). Examples of transitional forms include Orthrosanthus chimboracensis (RudalI1984), in which the PTM is persistent for some distance away from the apex, and forms a 'woody' pericyclic vascular plexus, probably homologous with the secondary vascu• lar tissue of some other Iridaceae, such as Patersonia. Chlorophytum suffruticosum (this paper) also has a persistent PTM, and Thysanotus spiniger probably an STM, as the vascular derivatives are extensive. In contrast with other monocotyledons, the asparagoid PTM often extends many internodes away from the apex. For example, there are numerous records of PTMs producing extensive radial derivatives in asparagoid bulbs, such as in Scilla (Chouard 1936), Polyanthes (Chakraverti 1939), Eucomis (Reyneke & Van der Schijff 1972), Allium (DeMason 1979) and Tigridia (RudalI1989). Bulbs are mainly found in the asparagoid clade among monocotyledons, and the

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Table l. Taxa recorded as having an (unequivocal) STM. Families given as in Brummitt (1992).

Genus Reference

Agave Agavaceae Chouard (1936), Cheadle (1937), Lu & Chiang (1976) Aloe Cheadle (1937), Lu & Chiang (1976) Aphyllanthes Aphy llanthaceae Tomlinson (1965), Chakroun & m~bant (1983) Beaucarnea Nolinaceae Stevenson (1980) Cordyline Cheadle (1937), DeMas on & Wilson (1985) Dasylirion Nolinaceae Cheadle (1937) Dracaena Dracaenaceae Cheadle (1937), Zimmermann & Tomlinson (1970) Furcraea Agavaceae Cheadle (1937) Gasteria Asphodelaceae Tomlinson & Zimmermann (1969) Haworthia Asphodelaceae Tomlinson & Zimmermann (1969) Herreria Herreriaceae this paper Klattia Iridaceae Adamson (1925126) Lomandra Lomandraceae Fahn (1954), this paper Nivenia Iridaceae Adamson 1925126, 1930/31 (as Aristea) Nolina Nolinaceae Cheadle (1937) Patersonia Iridaceae Rudall (1984) Sansevieria Dracaenaceae Cheadle (1937) Thysanotus Anthericaceae this paper Trachyandra Asphodelaceae Adamson (1931) Witsenia Iridaceae Adamson (1925/26) Xanthorrhoea Xanthorrhoeaceae Cheadle (1937), Waterhouse (1967), Staff & Water• house (1981) Yucca Agavaceae Chouard (1936), Cheadle (1937), Diggle & DeMason (1983)

nature of the asparagoid PTM may account for this. The STM is, therefore, virtually restricted to the asparagoid clade, and several authors (e.g. Waterhouse 1987), have regarded it as an important character for the systematics of this group. However, many Asparagales lack an STM, indicating that it has either arisen more than once, or been lost several times. Recent analyses of Asparagales, both molecular (Chase et al. 1995) and morpho• logical (Rudall & Cutler 1995), show some consensus in presenting both a 'lower' asparagoid paraphyletic grade (i. e. several basal taxa) and a 'higher' asparagoid clade, although they vary in detailed topology. These results are not conclusive, since there are many missing data and taxa, and other analyses (e.g. Stevenson & Loconte 1995) produce conflicting results. However, they provide a useful basis for discussion and character analysis, and demonstrate that current family delimitation in this group, based on floral characters, is far from satisfactory. Among the 'lower' asparagoids, an STM occurs in some genera of Iridaceae (Klattia. Nivenia. Patersonia and Witsenia: Rudall

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1984). Isophysis, a Tasmanian endemic which is considered close to Iridaceae or in• cluded within it (Goldblatt et al. 1984), is unfortunately unknown for this character due to lack of available material. An STM is absent from all the asparagoid taxa below Iridaceae in the cladogram, including the Australian Doryanthes. Xeronema, a taxonomically isolated 'lower' asparagoid genus (with ensiform , as in Iridaceae) from and Poor Knights Island, also lacks an STM. An STM occurs in some taxa of Asphodelaceae, which is either placed among the 'higher' asparagoids, or at the top of the paraphyletic 'lower' asparagoids. Apart from Iridaceae and Aspho• delaceae, an STM occurs in about five separate clades of 'higher' asparagoids, inter• spersed with taxa without an STM. This distribution indicates that the STM has arisen more than once within the asparagoid clade. Since it is an almost uniquely asparagoid character, the most likely explanation is that these taxa are pre adapted to develop an STM, due to the relatively extensive PTM that is widespread amongst the group. In conclusion, although the presence of an STM may have some systematic value among small groups of genera (e.g. within Iridaceae), its absence cannot generally be regarded as evidence of relationship, and there are problems with the precise definition of the character. The presence of an STM in Herreria provides weak support for its relationship with a clade that includes Agave, Yucca and also Chlorophytum. The pres• ence of an STM in the Australasian genera Lomandra and Thysanotus supports other evidence from embryology (RudaIl1994) and rbcL (Chase et al. 1995) of a likely rela• tionship between them. There may well be more examples of herbaceous taxa with an STM, especially within the families Asphodelaceae and Agavaceae, since many spe• cies have not yet been investigated for this character. Possible candidates include Iso• physis (related to Iridaceae: see above) and Chamaescilla, Eustrephus, Sowerbaea and Trichopetalum, which all share characters with Lomandra and Thysanotus.

ACKNOWLEDGEMENTS

I am grateful to Janet Rusby (University of Bradford), for preparing microscope slides during her year of work experience at Kew.

REFERENCES

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