Nuclear Phenomena of Sexual Reproduction in Fungi
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NUCLEAR PHENOMENA OF SEXUAL REPRO- DUCTION IN FUNGI1 PROFESSOR R. A. HARPER -UNIVERSITY OP AWISCONSINT IhTthe light of recentresearches the old dogma that thme parasitic.mode of life tends to tlmedisappearance of sex- uality lhas practically disappeared at least so far as the fungi are concerned. Tlmeevidence is now generally ac- cepted that either a typical conjugation of normallydif- ferentiatedgametes and their nuclei or somimeform of sub- stitute for it is everywherepresemit. Ernst and Schmiidton tlmebasis of their studies on the root parasite Raqi7iesiahave also recentlyemphasized tlme fact that there is no evidence iii tihecase of seed plants that timeparasitic habit temidisto timedisappearance of .sexuality. Farmer and Digby have described a m-ost remarkable substitutefusion in an apoganmousfern and. a still miorestrikinog case of substitute cell and nuclear fusions in another apogam-iousferml has been recentlydis- covered in my own laboratory. It is proper under these conditions to examimimmeanew and most critically all cases of cell fusions with reference to their accompanying nuclear phenomena and possible significancein the life cycle in question. The study of sexuality in timefungi has also broughtto light some fundalameutalmoodifications of the process of' sexual fusion as found elsewhere which enlarge our con- ception of timenature and significanceof gamueticunions. It has also revealed most.curious and strikiingsubstitu- tions for sexual fusions. I shall review brieflythe most characteristicand significantof these variatiomisfrom the ordinary methodsof sexual reproduction. The fusion of 'A paper read by invitation before the Botanical Society of America, Boston, Decemnber30, 1909. 533 This content downloaded from 142.109.001.196 on February 18, 2018 20:56:27 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 534 THE AMERICAN AT-ATURALIST [VOL. XLIV the amceboids-warmspores to formthe plasmocliumof the slime moulclshas never been satisfactorilyaccounted for, nor related to the processes either vegetative or sexual in othergroups of fungi. With the increase of our kno-wl- edge of the possible variations -whichthe sexual process may undergo it is becoming more possible to accept the conceptionthat in some way the formationof the plas- modiurnmay representeither an incipientor an aberrant type of gamieticunion in which the normal fusion of two gametes is replaced by a massing of indefinitelynumer- ous cells. The cytological study of the group is only just begin- ning and doubtless,much is to be correctedin the frag- meentaryobservations already published. Olive, Jahln and Kra.enzlein,however, agree that there are evidences of nuclear fusions either just before spore formationor earlier in the formationof the fruitbodies, and that these karyogamies are. followed by synapsis and reduction divisions. The figures given show tha.t these forms have typically developed nuclei which are favorable for fixing and staining, and indicate that whatever disagreement exists as to what occurs ill the few types studied may be expected to be cleared up by furtherwork. The older authors were loath to regard the union of the amceboeto form a. plasmodium as involving anything of a sexual nature, but it is quite possible that we may have to extend our conceptionof sexual fusions at least in their primitiveforms to include cases of multiple cell fusions followed by vegetative <growth,and finally the fusion of the nuclei in pairs. That cell and nuclear fu- sions may be thus widely separated is plain from the conditionsin the rusts, and in the slime moulds, as in the rusts, nuclear fusion is followed shortlyby the reduction divisions. We can not yet regard the nuclear phenomena in the slime nmouldsas sufficientlycleared up. In the light of what has been found in other fungi there is however cer- taiinlyno ground for believing that the nuclear history This content downloaded from 142.109.001.196 on February 18, 2018 20:56:27 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). No. 525] SEXUAL REPRODUCTION IN FUNGI 535 in the plasniodiumnis as simple as the older students be- lieved. As directlysuggestive of what may be expected in the slime moulcds,we have the well-established fact of the fusing of multinucleated gametes and the subsequent pairing of all or approximately all their nuclei. Leger and othershave seen that the gametes of Sporodinia.and other zygomycetesare multinucleated,but the accounts of Ljo snblsegent -pocesses in the zvgospore Can not be accepted as well fou-ndedand ilo one vet ha-sbeen able to traceethe historyof these minutenuclear gram-iles. Stevens,however, has established the entranceof many male nuclei and their subsequentpairing with the numer- outsnuclei of the eggs of Cystopts bliti and port'dlaec( and unpublished observations made in my own labora- tory have confirmedhis results for C. bliti. I have also found such multiplefusions of about 9200nuclear pairs in the large oogonia,of Pyroniemjia.. Claussen in a prelini- nary paper, while confirmingthe existence of the fusion of multinucleatedgametes and subsequent pairing of the sexual nuclei in Pyronemna,claims. that the fusion of the pairs is not completedtill they reach the ascus. The large size of the nuclei in the ascogenous lhyphle in Claussen's preliminaryfigures seems to me, however, to confirmmV own conclusion that the fusion is already completed at this stage. These multinucleatedgametes prove convincinglythat our conlceptionof the egg and male cell must be extended to include multinucleatedas well as uniirucleatedctypes. The cell at the moment,of sexual union may be multinucleateda.s well as in its ordi- nary vegetative stages in the IyphTe, etc. That the nuclei fuse in pairs and not in larger numbersis further convincingevidence that they are the real bearers of the idioplasm and that the constancy of the chromosome num1- ber imustbe maintainedby the ordinaryty-,pe of doubling and subsequent reduction. With the demonstrationof the existence of coenocyftic gametes the nature of the coenocyteitself becomes still This content downloaded from 142.109.001.196 on February 18, 2018 20:56:27 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 536 THE AMERICAN NATURALIST [VOL. XLIV clearer, as I lhav-eelsewhere pointed out. The continuous plasma membraneenclosing a coenocyteis plainly in its relation to the other cell contents to be compared with the same structurein an uninucleateclcell ratherthan -with the aggregate of membraneswhich bound off a mass of tissue from its environmentand the cells of the tissue from each other. It is furthermost interestingto note that De Bary's conceptionof the male elementin the oomn-ycetesas gono- plasmn,a miereunbounded portion of the contentsof the antheridium,htas been entirely confirmedby subsequent cytologicalresearch, and it is furtherproof of the super- ior significanceof the nucleus as the carrier of the idio- plasmnin sexual fusions that in such forms as Cystopus Candid;11us,for example, it is merely one of the several nuclei in the anthericlium,and that with no definitely limited cyTtoplasmnicunit which migrates throughlthe eonljugationtube and fertilizesthe egg. The differentia- tion of the male gamete is not here an ordinary process of cell division, but a mere flowing out of one of the nuclei of the coenocv-ticantheridiumi. The most strikingdiscovery as to fusion in the fungi and the one whichpreceded and led the way to very many of the more importantlater results was the observation by Wager of paired nuclei and the subsequent fusion of these nuclei in the young basiclium. \\ager was mistaken in describing a series of such fusions b)y\Tpairs, but the clear account of the nuclear structureswhich lie gave and the evidence that nuclear division occurs by a karyokinesislike that of other plants and animals showed for the firsttime the possibility of determiningthe nature of the various reproductivebodies in fungiby a more exact cytologicalinvestigation of them than had before been thought possible. Wager bro-Lght.the firstproof of the existence of an endokarvogamy- the fusion of nuclei not derived from separate and independent gametes as in ordinary fer- tilizations,but having had a similar if not identical his- This content downloaded from 142.109.001.196 on February 18, 2018 20:56:27 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). No. 525] ASEXUAL REPRODUCTION IN FUNGI 537 tory in the cells fromwhich the basiclium a-rose. Such a process was entirelyunknown before in either plants or animals. Subsequent investigations by Daugeard, MNlaire, Buh- land, Nichols, myself and others have shown that iii the Basidiomnvcetesa lonogseries of binucleated cells, pre- cedes the formation of the basiclinunand the nuclear fusion in it may well have somethingof the value of a union of differentiatedgamietic nuclei. Tbe origin of the binucleated cells in the Basidiomiy- cetes does not apparently result from a cell fusion at a definitepoint in the life cycle, as is the case in the Tcid- iuni of the rusts. Such a fusion might perhaps be ex- p)ected to be effectedat the origin of the carpophore,but it has been established that binucleatecl cells may be present in the m'iyceliumprior to the formation of the ca rpophore. Series of such cells may extemdclback almost if miotquite to