Generic Placement of Species Excluded from Arabidopsis (Brassicaceae)

Abstract

All 59 binomials previously assigned to Arabidopsis are critically evaluated and placed in 14 genera, of which Crucihimalaya, Olimarabidopsis, and Pseudoarabidopsis are described as new. Nine new combinations in Crucihimalaya, three in Olimarabidopsis, and one in Pseudoarabidopsis, as well as 12 new synonyms, are proposed. A key to all genera most commonly confused with Arabidopsis, including the three new proposed herein, is presented. Generic delimitation in the Brassicaceae (Cruciferae) is one of the most difficult and often controversial aspects in the systematics of the family (Al-Shehbaz, 1973, 1984; Rollins, 1993; Schulz, 1936). Perhaps the two principal reasons for this are: (1) Convergence in basically every morphological character is so high that superficially very similar genera might well turn out to be remotely related or unrelated upon critical examination of so-called key generic characters and independent assessment of phylogenetic relationship using molecular comparisons (as in the genera herein segregated from Arabidopsis). (2) Although the family exhibits tremendous diversity in fruit morphology, other parts of the plant, especially the flowers, usually do not show much diversity and, therefore, there are few morphological characters that can be used to determine relationships. Characters of flowers and vegetative parts have often been ignored or overlooked. Because fruit morphology has traditionally been used in taxonomic treatments of the Brassicaceae, the problem becomes more acute among the numerous genera with relatively similar linearshaped fruits. In cases like these, vegetative or floral characters could easily be of greater significance than fruit or seed characters in delimiting natural genera. Given the great interest in Arabidopsis thaliana (L.) Heynhold as a model experimental organism, it is of particular value to define clear phylogenetic groupings among its related genera. The limits of Arabidopsis (DC.) Heynhold have been the subject of continuous controversy, and many authors (e.g., Al-Shehbaz, 1988; Hedge (in Hedge & Rechinger), 1968; Price et al., 1994) called for the need to establish well-defined boundaries between the genus and its relatives. Although O'Kane and AlShehbaz (1997) retained only nine species in Arabidopsis, the generic placement of 50 of the 59 binomials previously assigned to Arabidopsis remained to be established. The present paper addresses this problem, and keys for the determination of taxa most often confused with Arabidopsis are provided. Molecular comparisons of both chloroplast DNA (Price et al., 1994, unpublished) and nuclear Internal Transcribed Spacer (ITS) regions (O'Kane et al., 1995, 1997, unpublished) have consistently supported dividing the core group of the broadly circumscribed Arabidopsis (e.g., table 1 of Price et al., 1994) into a small number of well-separated clades, most notably Arabidopsis sensu stricto (including Hylandra A. Love and Cardaminopsis (C. A. Meyer) Hayek; see O'Kane & Al-Shehbaz, 1997; Mummenhoff & Hurka, 1995), A. pumila (Stephan) N. Busch and relatives (here newly described as Olimarabidopsis), and A. himalaica (Edgeworth) O. E. Schulz and relatives (here newly described as Crucihimalaya). All of these genera belong to a major terminal clade, including a number of other Eurasian and American genera such as Capsella Medikus, Neslia Desvaux, Erysimum L., Malcolmia R. Brown, and Halimolobos Tausch. Several other species sometimes placed in Arabidopsis have been found to belong to the distantly related genera ThelNOVON 9: 296-307. 1999. This content downloaded from 157.55.39.78 on Fri, 24 Jun 2016 05:14:10 UTC All use subject to http://about.jstor.org/terms Volume 9, Number 3 1999 Al-Shehbaz et al. Exclusion from Arabidopsis 297 lungiella O. E. Schulz (Al-Shehbaz & O'Kane, 1995; Galloway et al., 1998) and Neotorularia Hedge & J. Ldonard (Al-Shehbaz & O'Kane, 1997), or in one case to the genus Erysimum (Al-Shehbaz, 1994), which is closely related to Olimarabidopsis. Although the taxonomy of Arabidopsis has now been worked out at the generic level (O'Kane & Al-Shehbaz, 1997), our research indicates that Arabis is polyphyletic and consists of at least three unrelated clades. Following up the suggestions of new phylogenetic groupings provided by molecular comparisons, we have thoroughly reexamined the morphology of the species previously placed in Arabidopsis in order to reassess morphological groupings of species and to try to find morphological characters distinguishing the groups indicated by molecular comparisons. Over the last seven years, we have critically examined more than 6000 specimens from numerous herbaria. We have found that differences in fruit morphology (terete vs. flattened) and seed morphology (incumbent vs. accumbent cotyledons and winged vs. unwinged seeds), which have been previously used (e.g., Busch, 1909; Ball, 1993; Jones, 1964; Mulligan, 1995; Rollins, 1993; Schulz, 1936) to separate the traditionally circumscribed genera Arabidopsis and Arabis, appear to be very unreliable in the delimitation of natural generic groups. Seven of the nine species of Arabidopsis sensu stricto have flattened fruits and accumbent cotyledons, while two have terete fruits and incumbent cotyledons (O'Kane & Al-Shehbaz, 1997). In contrast, differences in trichome branching, flower color, and nature of the cauline leaf base appear to be much more useful in defining natural generic groups among species previously placed in Arabidopsis sensu lato. Combinations of these characters, along with molecular phylogenetic data, support the retention of 9 species in Arabidopsis and the segregation of 13 species commonly placed in the genus into three new, well-defined genera herein proposed as Crucihimalaya, Olimarabidopsis, and Pseudoarabidopsis. Based on chloroplast DNA sequencing (Price, unpublished), Olimarabidopsis is most closely related to Erysimum, and both are readily separated from Arabidopsis by having yellow or orange (rarely cream or purplish) flowers and malpighiaceous and/or sessile stellate trichomes (Erysimum) or submalpighiaceous and subsessile stellate trichomes (Olimarabidopsis). Only 3 of the 14 genera to which the 59 Arabidopsis binomials belong are not included in the following key. These, Murbeckiella Rothmaler, Sisymbriopsis Botschantsev & Tzvelev, and Robeschia Hochstetter, are unrelated to Arabidopsis. Murbeckiella has auriculate cauline leaves, keeled valves, veined septa, and winged seeds, whereas Arabidopsis has petiolate cauline leaves, rounded or flat valves, veinless septa, and wingless seeds. Sisymbriopsis has pubescent, quadrangular fruits and prominently 3-veined valves, whereas Arabidopsis has glabrous, terete or flattened fruits and veinless or obscurely 1-veined valves. Finally, Robeschia has dendritic trichomes, 2-pinnatisect or 2-pinnate leaves, much thickened fruiting pedicels as thick as the fruit, and an obsolete style, whereas Arabidopsis has simple and stalked forked trichomes, undivided to pinnatifid leaves, slender fruiting pedicels narrower than the fruit, and distinct styles. These three genera have not yet been subjected to molecular studies, but should be analyzed in the near future. The circumscriptions of Arabis and Halimolobos in the following key follow that of Rollins (1993). We are, however, aware that these genera, as presently delimited, represent very heterogeneous assemblages of species groups that will have to be re-assigned to other genera, most of which have already been proposed. We are currently working on these groups. ARTIFICIAL KEY TO THE GENERA WITH MEMBERS FORMERLY PLACED IN ARABIDOPSIs SENSU LATO la. Plants completely glabrous; leaves and stems glaucous; plants often restricted to strongly saline and/or calcareous soil Thellungiella lb. Plants sparsely to densely hairy; leaves and stems not glaucous; plants usually on other soil types. 2a. Trichomes sessile and completely appressed, malpighiaceous and/or stellate with unbranched rigid straight rays Erysimum 2b. Trichomes shortor long-stalked, simple or branched, if stellate and sessile then rays slender and/or branched. 3a. Scapose annuals without cauline leaves; fruiting pedicel nearly as thick as fruit ....... Drabopsis 3b. Nonscapose annuals, biennials, or perennials with few to many cauline leaves; very rarely perennials without cauline leaves; fruiting pedicels much narrower than fruit (except some Neotorularia). 4a. Fruits compressed; cotyledons accumbent. 5a. Cauline leaves short petiolate, neither auriculate nor sagittate at base; trichomes simple and 2or 3(or 4)-forked, never dendritic or stellate; fruit valves with a prominent midvein; seeds usually wingless .Arabidopsis This content downloaded from 157.55.39.78 on Fri, 24 Jun 2016 05:14:10 UTC All use subject to http://about.jstor.org/terms