NEWS & VIEWS COMMENTARY AMERICAN JOURNAL OF BOTANY E VOLVING WORDS AND THE EGG-BEARING TUBES OF 1 W ELWITSCHIA (WELWITSCHIACEAE) W ILLIAM E. FRIEDMAN 2 Department of Organismic and Evolutionary Biology, 26 Oxford Street, Harvard University, Cambridge, Massachusetts 02138 USA; and Arnold Arboretum of Harvard University, 1300 Centre Street, Boston, Massachusetts 02131 USA Key words: alternation of generations; gametophyte; Gnetales; prothallial tubes; seed plants; Welwitschia . In 1863, Joseph Hooker published the fi rst monographic extensions of the female gametophyte of Welwitschia did in- study of Welwitschia , a species that had only recently become deed involve an author’s explicit attempt to render a state- known to science ( Friedman, 2015 ). In the process of studying ment of homology with developmental and evolutionary its reproductive biology, Hooker discovered that the female ga- implications. metophyte produced an unusual set of tubular extensions at the Early in its development, the female gametophyte of Wel- micropylar pole that he called “secondary embryo-sac tubes.” witschia differentiates into two distinct regions: a large chalazal Over the course of the next century and a half, these apomor- domain that is vegetative in nature and a smaller micropylar phic structures were renamed more than a half dozen times by domain that will ultimately supply female gametes to the fertil- various workers. Commonly, these structures have been re- ization process ( Friedman, 2015 and references therein). These ferred to as “prothallial tubes.” During the review process for two domains are initiated from the single-celled coenocytic my paper on female gametophyte development, gamete forma- stage of the gametophyte, which is cleaved into a number of tion, and fertilization in Welwitschia ( Friedman, 2015 ), the smaller multinucleate cells. The chalazal domain is made up of question was raised (by the reviewers), what is the appropriate cells that contain roughly a half dozen to a dozen free nuclei. appellation for these unusual structures? The nuclei within each of these cells will then fuse into a single Here, I address the issue of the historically and botanically large polyploid nucleus, and this tissue will go on to develop appropriate term for these remarkable egg-bearing out- into the main embryo-nourishing tissue within the seed. At the growths of the female gametophyte of Welwitschia . The most micropylar end of the coenocytic female gametophyte, clues stretch back more than a century and a half in the En- cellularization also produces a set of multinucleate cells, but glish, French, and German language botanical literature and these cells usually contain fewer than fi ve nuclei. Unlike the involve a cast of botanical luminaries including Wilhelm chalazal domain coenocytic cells (that become uninucleate), the Hofmeister, Joseph Hooker, Eduard Strasburger, John Coul- micropylar-most coenocytic cells remain multinucleate. Each ter, Charles Chamberlain, Karl Goebel, Karl Schnarf, Pierre micropylar coenocytic cell then initiates a tubular growth up Martens, and Ernest Gifford. Unlike taxonomy, where no- into the nucellus, that Hooker (1863) fi rst described and called menclatural rules govern the assignment and codifi cation of “secondary embryo-sacs.” These tubes bear free nuclei, some taxon names (of course, not without controversy and debate), of which will differentiate into eggs and be fertilized when the naming of structures in plant morphology and embry- these tubular extensions meet and fuse with the tips of ology is not codified. Often, however, in the naming of downward growing pollen tubes in the midst of the nucellus morphological and embryological structures in plants, a ( Pearson, 1909 ; Martens, 1971 ; Martens and Waterkeyn, 1974 ; statement of homology assessment is implied. As will be Friedman, 2015 ). seen in this commentary, each attempt to name the tubular Since their discovery, these gamete-bearing tubular exten- sions of the female gametophyte have been variously referred to as “secondary embryo-sacs” and “secondary sacs” ( Hooker, 1 Manuscript received 17 December 2014; revision accepted 9 January 1863 ), “Corpusculum schlauches” ( Strasburger, 1872 ), “arche- 2015. gonial tubes” ( Coulter and Chamberlain, 1901 ), “prothallial The author thanks David Haig (Harvard University) for the introduction tubes” ( Pearson, 1906 ), “embryo-sac tubes” ( Pearson, 1909 , to Google Ngram and Judy Jernstedt (University of California, Davis), 1929 ), “Prothallienschläuche” ( Goebel, 1932 ), “Embryosack- Editor-in-Chief of the American Journal of Botany , for her expert handling of this manuscript. This research was supported by a grant from the schläuche” ( Schnarf, 1933 ), “egg tubes” ( Battaglia, 1951 ), National Science Foundation (IBN-9696013) to W.E.F. “tubes endospermiques” ( Martens and Waterkeyn, 1974 ) and 2 E-mail: [email protected] “endospermic tubes” ( Martens and Waterkeyn, 1975 ), or “ga- metophytic tubes” and “female gametophytic tubes” ( Gifford doi:10.3732/ajb.1400537 and Foster, 1989 ). The nomenclatural history of these tubes American Journal of Botany 102 ( 2 ): 176 – 179 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America 176 FRIEDMAN—EVOLVING WORDS AND WELWITSCHIA • VOL. 102 , NO. 2 FEBRUARY 2015 • 177 turns out to be long and complicated, but also extremely illumi- fertilization in angiosperms ( Nawaschin, 1898 ; Guignard, nating of the evolving meanings of botanical terminology over 1899 ), Pearson (1909) viewed the endosperm (meaning the the last 175 years. During this time, the alternation of genera- embryo-nourishing tissue) derived from these cells in Wel- tions would be discovered, the basic processes of fertilization witschia as an evolutionarily novel organism, which he named and syngamy would be illuminated across land plants, the re- a “trophophyte”. ductive divisions of meiosis would be revealed, and the sexual In 1910, Coulter and Chamberlain accepted Pearson’s 1906 origin of endosperm in fl owering plants (from double fertiliza- terminology, in the process rejecting the notion that these tubes tion) would be discovered. It is little wonder that the history of were homologous with or derived from archegonial initials terminology associated with the gametophytic structures of (sensu Strasburger), and referred to these structures as prothallial Welwitschia refl ect the complexities of ever-expanding knowl- tubes. Buchholz (1922) , in his classic paper on gametophytic and edge of the plant reproductive process and the never static evo- gametic competition (“developmental selection”) in plants, also lution of the meaning of words from the mid-19th century into used “prothallial tubes” in his discussion of Welwitschia . the 20th century. Pearson (1929) , in his posthumously published fi nal words on Hooker (1863) , the first person to see and describe the the topic rejected the suggested homology of the tubular struc- micropylar tubular outgrowths of the female gametophyte of tures that grow from the micropylar apex of the female gameto- Welwitschia , referred to them as secondary embryo-sacs or phyte of Welwitschia with an archegonium and continued to secondary sacs. Throughout the latter half of the 19th century favor embryo-sac tubes as the appropriate name. The explicit and early 20th century, “embryo sac” was used to refer to the homology of the micropylar tubular outgrowths of the female female gametophyte of any seed plant, not solely those of an- gametophyte of Welwitschia to an archegonium was also strongly giosperms, as is currently the case. Strasburger (1872) who was rejected by Schnarf (1933) , who settled on the literal translation the next to examine the gametophytes of Welwitschia referred of Pearson’s (1929) embryo-sac tubes (Embryosackschläuche). to these outgrowths as Corpusculum schlauches (corpusculum In Chamberlain’s (1935) classic work Gymnosperms, Struc- tubes), “corpusculum” being used in the latter half of the 19th ture and Evolution , the term prothallial tubes was resurrected, century to indicate an archegonium in gymnospermous seed and this nomenclature was followed by Sporne (1965 , The plants (for example, see Hofmeister, 1851 , 1862 ). This usage Morphology of Gymnosperms ) and Singh (1978 , Embryology and homology assessment was then picked up by Coulter and of Gymnosperms ). Foster and Gifford (1959 , 1974 , Compara- Chamberlain (1901 , p. 126), who stated that in Welwitschia tive Morphology of Vascular Plants ) reverted to the term em- “each archegonial cell develops a long tubular process.” A half bryo sac tube in the fi rst and second editions, as did Bierhorst century later, Battaglia (1951 , p. 94) would argue that the tubes (1971) in Morphology of Vascular Plants . Drawing on the older of Welwitschia “may be considered homologous to an archego- usage of the term endosperm (originally a physiologically de- nial initial” and suggested the appellation egg tubes. Interest- fi ned term relating to the tissue that acquires nutrient reserves ingly, Sterling (1963 , p. 184) argued that the prothallial tube of for the embryo within a seed—and derived from usage that pre- Welwitschia “is the homologue of an archegonium” and then dates the discovery of double fertilization and the sexual origin extended this case to suggest that the pollen tube is the homo- of angiosperm endosperm, as opposed to the nonsexual origin logue of an antheridium. of the female gametophytes of gymnosperms), Martens and In his original paper on female gametophyte development