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1 [310] MEIOSIS IN DIPLOID AND TRIPLOID HEMEROCALUS BY S. O. S. DARK John Innes Horticultural Institution, Merton (With 9 figures in the text) THE object of the present study is to give an account of the structure of the paired chromosomes seen during the later stages of meiosis in Hemerocallis and to show how the configurations that are observed in the meiotic division of a non-hybrid triploid plant can be related to those occurring in the reduction division of an ordinary diploid one. MATERIAL AND METHODS The chromosome numbers of the following species and varieties of Hemerocallis were examined in root tip mitotic divisions and where possible in pollen mother cell divisions for meiosis. Root tips were fixed in 2BE and cut at a thickness of ZOJJL. The sections were then stained by Newton's gentian-violet method. Pollen mother cells were fixed by the smear method. Medium Flemming, Benda and 2BE were employed as fixatives, gentian-violet being used for staining (vide La Cour, 1931). LIST OF SPECIES, ETC., EXAMINED Diploid. Hemerocallis aurantiaca Bak. (pollen mother cells). H. fulva L. H.fulva X H.fiava. H. fiava L. (pollen mother cells). H. Middendorfii Traut. et Mey. H. Elmusae (pollen mother cells). 1 Plants received under these H. hippeastrioides names from the Elwes col- H. vermusae (pollen mother cells), j lection. Mr J. E. Dandy of the British Museum kindly informs me that he can trace no authority for these names. Triploid. H. fulva var. Kwanso Regel (pollen mother cells).
2 Meiosis in Diploid and Triploid Hemerocallis 311 All the forms were diploid, with a chromosome number of 2«= 22, except H. fnlva var. Kwanso, which bears double flowers having no female organs and is a triploid clone with 33 chromosomes. These numbers agree with those given by Takenaka (1929), except that his H. fulva was also a triploid while mine was diploid, and is evidently the type from which the triploid arose. The somatic chromosomes throughout the species examined were of very similar types. Individual chromosome forms were not recognisable, but types could be distinguished. Each complement contains three pairs of long chromosomes with median or sub-median attachment constrictions and from two to four pairs with sub-terminal attachments (Figs, i, 3, 4, 7 and 9). MEIOSIS Satisfactory prophase stages of meiosis could not be obtained in this material. Even at diakinesis the chromosomes are too condensed for observation of fine details of structure (Fig. 2). At metaphase the chromosomes present a characteristic appearance in side view of the equatorial plate of the spindle. In the diploid species the chromosomes all pair to form ii bivalents, while in the triploid variety Kwanso trivalents, bivalents and univalents occur. The configurations seen at metaphase can all be explained by the theory that the pairing of homologous chromosomes at metaphase and the maintenance of their association until anaphase is conditioned by the formation of chiasmata (Darlington, 1931 c). Each chromosome is longitudinally split into two half-chromosomes or chromatids and a chiasma is formed between homologous chromosomes by an exchange of partners among these chromatids, which always associate in pairs. The shape of each configuration is determined by the number and position of the chiasmata present in conjunction with the position of the attachment constriction on the paired chromosomes. In the majority of organisms these chiasmata are formed more or less at random along the lengths of the paired chromosomes at the diplotene stage of meiosis. As prophase proceeds, the forces of repulsion acting between the attachment constrictions compel the chiasmata to travel towards the distal ends of the chromosomes, i.e. terminalisation occurs, often giving end-to-end association of the chromosomes by "terminal chiasmata." This may result in {a) reduction of the number of chiasmata by telescoping them at the chromosome ends to form terminal chiasmata, or [b) merely pushing
3 Fig. I. Somatic chromosomes in root-tip divisions oi Henwrocattis spp. Top left: H.fiilva. Top right: H. flava. Bottom: Hybrid H. fulva -H.flava Fig. 2. Diakinesis in H. flava. showing the condensed form of the bivalents.
4 Meiosis in Diploid and Triploid Hemerocallis 313 the distal interstitial chiasmata along to the ends to form terminal chiasmata, while the interstitial loops adjust their relative sizes, tending towards a state of equilibrium (cf. Darlington and Dark, 1932). In Hemerocallis as in the majority of flowering plants the chromosomes at metaphase are sometimes too small and condensed to demonstrate chromatids and chiasmata directly. In these cases we can, however, infer that these structures are responsible for the observed configurations: (i) By analogy with similar configurations found in more favourable material in which the structure can be followed in detail. (ii) By study of the forms shown by the separating homologous chromosomes at anaphase. A test of the correctness of this inference is that on the basis of the mechanics of chromatid and chiasma behaviour, predictions of possible configurations can be made and these are verified by the finding of the configurations during the study of meiosis in various organisms, such as in the case of Oenothera which was formerly believed to have association of chromosomes only end to end ("telosynapsis"), an assumption now no longer tenable (Darlington, 1931 b; Catcheside, 1931 a, h). Fig. 3 shows a side view of a metaphase plate in which the bivalents have been separated laterally in drawing. Below is a diagram of the chromatid structure represented in the bivalents. Here it will be seen that all the chiasmata are either terminal or sub-terminal. In the division represented in Fig. 4 the first and eighth bivalents from the left-hand side have both terminal and interstitial chiasmata as shown in the chromatid diagrams below. The thin threads in the bivalents may be supposed to be due to the forces of repulsion, already assumed to act between the attachment constrictions in terminalisation, being strong enough to stretch the chromatin material. This happens where a chiasma occurs close to the attachment constriction, which is more usual in short bivalents. The stretching continues until at anaphase the chromatids distal to the chiasma holding the bivalent together come apart and allow the chromosomes to separate as they move towards the poles. As they come apart from each other the tension is released and the chromatids snap back as if they were elastic to form small projections (see Fig. 9, rightmost pair of chromosomes). The length of these separate arms depends upon the length of the chromatids, in the original bivalent, that was distal to the chiasma, for these portions of the chromatids
5 314 S. O. S. DARK are separate at anaphase wliile the proximal parts are closely paired and stuck together. This process is illustrated in Fig. 5, which shows successive stages in the unravelling of similar bivalents from meta- ^ AJhJlAJlJlll I ^ i ' ^ - s ^ i S i Q i o t i Fig. 3. H. verniusae. Top: metaphase of mitosis in somatic division. Middle: side view of metaphase I in meiosis. For clearness the bivalents are spaced out laterally in drawing. Bottom: line diagram of the metaphase I bivalents showing the chromatid interpretation of their structure. The repulsion between the attachment constrictions is indicated by the arrows. phase to telophase, and in Fig. 6 showing anaphase of a complete nucleus with chromatid diagrams of the important types. Type A is derived from the metaphase configuration shown in Fig. 5; B comes from a configuration like No. 2, Fig. 3, but differing
6 Meiosis in Diploid and Triploid Hemerocallis 315 from it in having a sub-ferminal chiasma in the left arm (cf. No. 6); C is given by No. 7, Fig. 3; D arises from No. i. Fig. 3; while E results from the bivalenfs represented in Fig. 3 as Nos. 5, 8,10 and 11. The size of the bead of chromafin between the two members of a bivalent is an indication of how nearly terminal is the chiasma, for the bead consists of the distal arms of a sub-terminal chiasma, hence the longer the arms the bigger is the bead. Fig 4 H atimntiaca. Top; somatic division. Middle : side view of metaphase I in meiosis Bottom; hne diagram of the chromatid structure of the first and eighth bivalents from the left in the metaphase shown above. X3750. THE TRIPLOID H. fulva var. Kwanso Examination of metaphase in the triploid showed univalents to be present in au cells, so that the occurrence of ri trivalents must be a very rare phenomenon. BeUing (1925) illustrates this condition in side view and Takenaka (1929) gives a not very convincing polar view
7 3i6 S. O. S. DARK of a cell with ii trivalents, and remarks on the rarity of complete trivalent formation. Generally there are 5 or 6 trivalents present with 6 or 5 univalents and bivalents. Only two of the four po.ssible configurations of three chromosomes with complete terminalisation have been.seen (Darlington, ic)3i a); these are the chain formation. laa Fig. 5- A Fig 5. H. aurantiaca. Three similar bivalents at metaphase I, anaphase I and telophase I of meiosis, showing stages in the unravelling of a chiasma, with line diagrams of the respective chromatid structures below. ;<375O. Fig, 6. H. aurantiaca. Anaphase I of the meiotic di\-ision with line diagrams bflow of the chromatid structures of the lettered bivalents. X3750. involving two simple terminal chiasmata (Fig. 8, ist, 2nd, 4th and 6th trivalents) and the "i'-trivalent, where all three chromosomes meet in a "triple chiasma," which is produced by terminalisation in the same direction of two interstitial chiasmata between three chromosomes (Fig. 8, 3rd and 5th trivalents). The triple chiasma type
8 Meiosis in Diploid and Triploid Hemerocallis 317 is formed when the chromosomes have terminal or sub-terminal attachment constrictions. The non-appearance of the more complicated trivalent configurations may be accounted for in two ways: (i) They may have been present but not distinguishable at metaphase. In the case of triploid Primula sinensis this was so, for although the frying-pan trivalent configuration was the commonest observed at diakinesis, only very few were seen at metaphase (Dark, 1931). (2) The chiasma frequency at diplotene may be very low, so that there is only an extremely small chance of getting more than two chiasmata between three chromosomes. Further, the chromosomes that form these configurations Fig. 7. H. Middendorfii. Top: metaphase of mitotic division. }3ottom: side view of metaphase I of meiotic division. X3750. must have nearly median attachment constrictions and in Hemerocallis there is apparently some peculiarity of prophase pairing by which this type often tends to form a ring bivalent and univalent instead of one trivalent. Metaphase pairing was formerly considered to be directly due to affinity between homologous chromosomes. In a non-hybrid clone such as thisi, each individual possesses three similar sets of chromosomes. Hence, on this assumption, as pairing is complete in the 1 The clone is considered by systematists to be a variety of the diploid species H. futva which it resembles in appearance. Since no tetrap oid /f.m.rocalus species are known, the triploid must have arisen by the functioning of an unreduced gamete and not by hybridisation.
9 3i8 S. O. S. DARK diploid, the triploid should have regularly ii trivalents or perhaps none at all, depending on the " strength of the affinity." The fact that a varying number of trivalents is formed could not be predicted upon this affinity assumption, but is to be expected according to the theory \\ I'ig. 8. H. fulva var. Kwanso. Top: metaphase of niitotic division. Middle: side view of metaphase I of meiosis. Bottom: hne diagram of chromatid structure fif the trivalent configurations shown in the figure above. The third and fifth from the left each have a triple chiasma. X3750. that metaphase association is due to chiasma formation between the parts of chromosomes paired at zygotine. For in a triploid, at zygotene, only two chromosomes are associated at any one point (Darlington, 1931 c). Hence if the association between two members of a set of three homologous chromosomes was very e.xtensive, the
10 Meiosis in Diploid and Triploid Hemerocallis 319 chances of a chiasma forming between the free portion of one and the third chromosome would be correspondingly reduced and a bivalent and univalent would be the result (Darlington and Mather, 1932). Micro-nuclei are formed in the pollen mother cell divisions and produce irregular "tetrads" containing various numbers of pollen grains. As Takenaka states, these arise from stray chromosomes. Since the metaphase chiasma frequency is low, one rarely meets with configurations that are lagging in their anaphase separation owing to difficulty in the unravelling of complex arrangements of chromatids, and only occasionally can lagging univalents be seen dividing on the equatorial plate after the other chromosomes have travelled to the Fig. 9. H. futva var. Kwanso. Anaphase I of meiotic division. X3750. poles in telophase. The formation of micro-nuclei appears to be chiefly due to metaphase univalents being situated too far from the equatorial plate to be included with the other chromosomes as they separate at anaphase. Hence at interphase they form nuclei of their own. SUMMARY AND CONCLUSIONS The present account shows that the structures of the pairing chromosomes in Hemerocallis can be explained in terms of the relationship of the chromatids (longitudinally split chromosomes) at chiasmata, and their behaviour at anaphase can be interpreted on the same basis.
11 320 S. O. S. DARK The failure of pairing of the third chromosome of each kind in the triploid clone (which is variable) can be regarded as due to the failure of chiasma formation (which is also variable), in the manner required by the chiasma theory of metaphase pairing. In no other way evident at present can this result be predicted. I am deeply indebted to Dr Darlington for his help and advice throughout this study. REFERENCES BELLING. J. Chromosomes of Canna and Hemerocallis. Jotirn. Hered. 16, CATCHESIDE, D. G. (a) Meiosis in a triploid Ooiothera. Jmirn. Genet. 24, (il) Critical evidence of parasynapsis in Oenothera. Proc. Roy. Soc. B, 109, DARK, S. O. S. Chromosome association in triploid Primula smensis. Journ. Genet. 25, DARLINGTON, C. D. (a) Meiosis in diploid and tetraploid Primula siiiensis. Journ. Genet. 24, [b] The cytological theory of inheritance in Oenothera. Journ. Genet. 24, (c) Meiosis. Btol. Rev. 6, DARLINGTON, C. D. and DARK, S. O. S. The origin and behaviour of chiasmata. II. Stenobothrus parallelus. Cytologta, Z, DARLINGTON, C. D. and MATHER, K. The origin and behaviour of chiasmata. III. Triploid Tulipa. (In the press.) LA COUR, L. Improvements in Everyday Technique in Plant Cytology. Journ. Roy. Micros. Soc TAKENAKA, Y. Karyological studies in//emftocawjs. Cytologia, 1, J
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