Research Article |
Corresponding author: Christopher T. Martine ( ctm015@bucknell.edu ) Academic editor: Sandy Knapp
© 2019 Angela J. McDonnell, Heather B. Wetreich, Jason T. Cantley, Peter Jobson, Christopher T. Martine.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
McDonnell AJ, Wetreich HB, Cantley JT, Jobson P, Martine CT (2019) Solanum plastisexum, an enigmatic new bush tomato from the Australian Monsoon Tropics exhibiting breeding system fluidity. PhytoKeys 124: 39-55. https://doi.org/10.3897/phytokeys.124.33526
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A bush tomato that has evaded classification by solanologists for decades has been identified and is described as a new species belonging to the Australian “Solanum dioicum group” of the Ord Victoria Plain biogeographic region in the monsoon tropics of the Northern Territory. Although now recognised to be andromonoecious, S. plastisexum Martine & McDonnell, sp. nov. exhibits multiple reproductive phenotypes, with solitary perfect flowers, a few staminate flowers or with cymes composed of a basal hermaphrodite and an extended rachis of several to many staminate flowers. When in fruit, the distal rachis may abcise and drop. A member of Solanum subgenus Leptostemonum, Solanum plastisexum is allied to the S. eburneum Symon species group. Morphometric analyses presented here reveal that S. plastisexum differs statistically from all of its closest relatives including S. eburneum, S. diversiflorum F. Meull., S. jobsonii Martine, J.Cantley & L.M.Lacey, S. succosum A.R.Bean & Albr. and S. watneyi Martine & Frawley in both reproductive and vegetative characters. We present evidence supporting the recognition of S. plastisexum as a distinctive entity, a description of the species, representative photographs, a map showing the distribution of members of the S. eburneum species group and a key to the andromonoecious Solanum species of the Northern Territory of Australia. This new species is apparently labile in its reproductive expression, lending to its epithet, and is a model for the sort of sexual fluidity that is present throughout the plant kingdom.
New species, andromonoecy, Solanaceae, Leptostemonum
As one of the most species-rich angiosperm genera (
The spiny solanums appear to have arrived in Australia some time in the last 5–10 million years (
The new taxon is the latest in a series of novelties from a set of taxa and forms within the “andromonoecious bush tomato” clade (
In this paper, we describe Solanum plastisexum Martine & McDonnell, sp. nov., a new species restricted to a small area in the central region of the Northern Territory of Australia that has confounded field botanists since at least the early 1970s. The few historical collections made of this taxon were especially confusing to Solanum experts (Fig.
Morphology and the earliest-known herbarium specimen of Solanum plastisexum. A Flowering stem with a single staminate flower in 2016 B Mature fruit C Erect inflorescences bearing staminate flowers in 2018 and D Specimen collected by P. Latz in 1974, held at DNA and annotated by D. Symon with an annotation indicating his confusion about the reproductive morphology of the specimen (male rachis visible above fruit on far left).
Fieldwork in Northern Territory during 2016 facilitated collection of specimens with male flowers and tissue for population genomic study (in prep), which has revealed that this new entity is an independently evolving lineage (unpublished data). The same population was visited again in 2018 and facilitated the collection of specimens with complete andromonoecious inflorescences (including both male and hermaphrodite flowers) and mature fruits with viable seeds, as well as information about population size, extent and local ecology. Specimens were examined from BUPL, DNA and NT (herbarium acronyms follow Index Herbariorum;
Field-collected seeds from two subpopulations were cultivated ex situ. First, seeds were soaked for 24 hours in 1000 ppm gibberellic acid solution in the dark at room temperature. Seeds were then sown in a growth chamber that was programmed to mimic an AMT climate and light regime at Bucknell University (Pennsylvania, USA) for approximately one month. Following successful growth, plants were cultivated in an IPM-managed greenhouse. Twenty-four vegetative and reproductive characters were measured from herbarium specimens and living plants. Characters were compared amongst six species that form a monophyletic group based on a recent phylogenetic and phylogenomic study (
Comparison of characters was conducted using JMP Pro 12 (SAS Institute, Inc., Cary, North Carolina, USA). Analyses included one-way ANOVA with Student’s t-test mean comparison at P < 0.05 and all the pairs by Tukey HSD to compare means and discern which species are different and in what way. A Connecting Letters Report was also generated to summarise mean values of each character across the six taxa included and to determine and assign significantly different sets when applicable. Multivariate morphometric analysis for all six taxa was also conducted using a principal components analysis (PCA) to place morphological variation in a spatial context.
ANOVA comparisons of each character along with Student’s t-tests and the Tukey HSD post-hoc comparisons reveal that species of this complex are, in large part, morphologically distinct (Table
The PCA score plot includes all measured characters and supports the relative distinctive nature of S. plastisexum when compared to the other taxa sampled. The analysis identified six eigenvalues above 1.0, which reveals that our dataset is roughly six-dimensional with principal components 1 and 2 contributing most of the variation amongst the points (47.8%). Figure
Principal components analysis score plot with eigenvalues and the contribution of each PC displayed (left) and loading plot (right) of characters and species in Table
Vegetative and reproductive characters measured for species included in this study along with associated means (M), standard deviations (SD), sample sizes (n) and connecting letters reports (CL). Different letters in the CL for each character indicates distinctions between species; species not sharing the same letter in a row are significantly different for that character (p < 0.5). All measurements in cm, except for seeds per fruit (n), seed length (mm), fruit wall width (mm), surface areas (cm2) and trichome densities (per 0.5 cm2). The term apical refers to expanded leaves near tips of growing stems, while the term basal refers to expanded leaves on lower parts of the stems. Connecting letters values in bold text for S. plastisexum indicate characters that statistically differentiate the species from its closest relatives.
S. diversiflorum | S. eburneum | S. jobsonii | S. succosum | S. watneyi | S. sp. nov. | |||||||||||||||||||
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Character | M | SD | n | CL | M | SD | n | CL | M | SD | n | CL | M | SD | n | CL | M | SD | n | CL | M | SD | n | CL |
Stem prickle length | 0.22 | 0.09 | 30 | D | 0.4 | 0.1 | 16 | A | 0.29 | 0.12 | 54 | BC | 0.37 | 0.07 | 20 | AB | 0.26 | 0.1 | 24 | CD | 0.38 | 0.12 | 25 | A |
Internode length | 2.23 | 0.91 | 30 | B | 2.16 | 0.67 | 16 | B | 1.48 | 0.51 | 54 | C | 3.6 | 0.73 | 25 | A | 4.01 | 0.98 | 24 | A | 1.48 | 0.43 | 25 | C |
Petiole length | 1.03 | 0.53 | 30 | D | 2.68 | 0.8 | 16 | B | 0.82 | 0.39 | 54 | D | 1.78 | 0.44 | 25 | C | 3.36 | 0.78 | 24 | A | 0.79 | 0.32 | 25 | D |
Apical leaf length | 2.66 | 0.77 | 25 | C | 11.32 | 1.83 | 16 | A | 5.39 | 1.33 | 25 | B | 5.13 | 1.09 | 25 | B | 12.39 | 2.51 | 24 | A | 4.97 | 0.89 | 25 | B |
Apical leaf width | 1.61 | 0.41 | 25 | B | 1.41 | 0.41 | 16 | BC | 1.69 | 1.13 | 25 | B | 1.84 | 0.53 | 25 | B | 2.47 | 0.65 | 24 | A | 1.06 | 0.22 | 25 | C |
Basal leaf length | 5.80 | 1.98 | 25 | D | 13.66 | 2.66 | 16 | B | 9.42 | 1.84 | 25 | C | 9.23 | 2.27 | 25 | C | 16.8 | 3.86 | 24 | A | 8.58 | 1.37 | 25 | C |
Basal leaf width | 3.24 | 0.91 | 25 | C | 2.03 | 0.88 | 16 | D | 4.97 | 1.54 | 25 | A | 4.56 | 1.17 | 25 | AB | 3.97 | 1.16 | 24 | BC | 1.59 | 0.37 | 25 | D |
Trichome density, adaxial, apical leaves | 81.6 | 48.28 | 5 | B | 419 | 125.27 | 5 | A | 121.0 | 61.42 | 5 | B | 345.0 | 43.36 | 5 | A | 138.33 | 20.26 | 3 | B | 482.2 | 79.82 | 5 | A |
Trichome density, abaxial, apical leaves | 162.4 | 82.84 | 5 | B | 453.2 | 103.03 | 5 | A | 156.40 | 47.65 | 5 | B | 412.6 | 63.31 | 5 | A | 206.0 | 20.78 | 3 | B | 491.6 | 79.01 | 5 | A |
Depth of lobing, apical leaves | 0.79 | 0.24 | 15 | A | 0.61 | 0.36 | 20 | AB | 0.9 | 0.62 | 15 | A | 0.91 | 0.4 | 25 | A | 0.27 | 0.36 | 10 | BC | 0.02 | 0.05 | 14 | C |
Depth of lobing, basal leaves | 1.48 | 0.38 | 15 | AB | 1.31 | 0.67 | 12 | B | 2.01 | 0.92 | 15 | A | 1.22 | 0.49 | 18 | B | 0.87 | 0.59 | 6 | B | 0.02 | 0.06 | 14 | C |
Surface area, apical leaves | 2.54 | 1.17 | 25 | C | 3.49 | 2.54 | 25 | C | 3.02 | 1.93 | 25 | C | 9.82 | 3.08 | 20 | A | 10.67 | 6.54 | 25 | A | 6.52 | 2.59 | 20 | B |
Surface area, basal leaves | 9.99 | 4.12 | 25 | B | 7.71 | 1.84 | 7 | B | 19.86 | 7.68 | 25 | A | 23.91 | 9.74 | 20 | A | 16.83 | 7.51 | 4 | AB | 11.63 | 6.58 | 11 | B |
Corolla diameter, male flowers | 2.24 | 0.45 | 16 | D | 3.5 | 0.31 | 15 | B | 3.02 | 0.44 | 23 | C | 3.11 | 0.34 | 25 | BC | 3.97 | 0.62 | 25 | A | 3.07 | 0.62 | 9 | BC |
Corolla diameter, hermaphrodite flowers | 2.96 | 0.37 | 16 | D | 4.12 | 0.35 | 13 | B | 3.58 | 0.5 | 17 | C | 3.77 | 0.45 | 17 | BC | 4.69 | 0.58 | 22 | A | 3.54 | 0.33 | 4 | BCD |
Calyx lobe length, male flowers | 0.35 | 0.09 | 15 | E | 0.69 | 0.06 | 3 | D | 1.16 | 0.14 | 10 | C | 0.17 | 0.02 | 25 | F | 1.13 | 0.14 | 7 | B | 1.63 | 0.03 | 3 | A |
Calyx lobe length, hermaphrodite flowers | 0.35 | 0.09 | 6 | D | 0.9 | 0.15 | 5 | C | 1.65 | 0.14 | 14 | C | 2.41 | 0.33 | 19 | A | 1.78 | 0.52 | 4 | B | 1.72 | 0.05 | 4 | B |
Pedicel length, in fruit | 2.7 | 0.18 | 13 | C | 3.64 | 0.93 | 14 | AB | 1.65 | 0.34 | 12 | D | 3.59 | 0.7 | 8 | AB | 4.16 | 0.72 | 17 | A | 2.94 | 0.47 | 9 | BC |
Fruit length | 3.11 | 0.29 | 14 | A | 1.8 | 0.29 | 13 | C | 1.65 | 0.13 | 3 | BC | 2.88 | 0.26 | 21 | A | 2.15 | 0.34 | 29 | B | 2.0 | 0.37 | 17 | BC |
Fruit width | 2.92 | 0.35 | 14 | A | 2.2 | 0.41 | 13 | B | 1.68 | 0.28 | 3 | B | 2.69 | 0.28 | 21 | A | 1.96 | 0.36 | 29 | B | 2.2 | 0.35 | 17 | B |
Seeds per fruit | 433 | – | 1 | A | 78.69 | 36.67 | 13 | C | 101.67 | 58.6 | 3 | C | 262.81 | 48.26 | 20 | B | 53.11 | 28.45 | 28 | C | 70.08 | 49.87 | 13 | C |
Seed length | 4.11 | 0.25 | 15 | A | 2.84 | 0.21 | 20 | C | 3.09 | 0.21 | 15 | C | 3.6 | 0.35 | 11 | B | 3.05 | 0.18 | 20 | C | 3.45 | 0.38 | 14 | B |
Fruit wall width | 4.4 | – | 1 | AB | 3.1 | – | 1 | AB | 2.20 | – | 1 | B | 4.22 | 0.51 | 6 | AB | 5.5 | – | 1 | A | 3.35 | 0.49 | 2 | AB |
Plant height | 33.8 | 5.35 | 3 | B | 43.62 | 10.86 | 16 | B | 34.08 | 7.3 | 6 | B | 69.2 | 27.03 | 5 | A | 45.85 | 6.91 | 24 | B | 77.33 | 2.52 | 3 | A |
Like Solanum eburneum, Solanum watneyi and Solanum succosum, but differing by having elliptic, unlobed (or rarely very shallowly lobed) leaves, small apical leaves, long calyx lobes on the staminate flowers and fully erect staminate inflorescence branches.
AUSTRALIA. Northern Territory: ~42 km E of Top Springs, on and around the Buchanan Highway, 16°42.274'S, 132°07.446'E, elev. 286 m, 23 May 2016 (fl, fr), C.T. Martine 4258, J.T. Cantley, L.M. Lacey, & P.C. Jobson (holotype: DNA; isotypes to be distributed to BM, BUPL, MEL, NY, PERTH)
Erect perennial herb 50–80 cm tall. Stems slender, woody at base, upright even when weighted by fruits; single stemmed, with some lateral branching on mature stems. Foliage and stems grey to grey-green, becoming slightly more yellow-green with age; indumentum of stems, leaves and inflorescences composed of stellate trichomes with the stalk, these short, appressed and very dense throughout (of Type 1 sensu
Solanum plastisexum is currently known from a restricted range on and around the Buchanan Highway in the sub-arid, monsoon-influenced zone of the northern region of the Australian Northern Territory (Figs
Nothing is known about the biotic interactions local fauna have with this species, although the floral morphology suggests the typical Solanum buzz pollination syndrome (
Map showing geographic distribution of all taxa compared in this study. red points = S. jobsonii, blue points = S. diversiflorum, black points = S. eburneum, pink points = S. watneyi, yellow points = S. succosum and purple asterisk = S. plastisexum. All points are based on specimens databased in the Australasian Virtual Herbarium (https://avh.chah.org.au/) and specimens held at BUPL.
The handful of collections that have been made of S. plastisexum that include flowers are all from the end of the wet season through the early months of the dry season, from January to June. Mature fruiting specimens have been collected in June.
The name is based on the Latin “plastus” (“deceptive,” but derived from the Greek “plastikos/plasticos/plasticus” for “able to be molded, changeable”) and the Latin “sexus” for sex. We suggest the use of Dungowan Bush Tomato for the common name of this species, which refers to the cattle station on which the majority of the collections have been made.
Solanum plastisexum is known from only two to three extant populations, each consisting of a few dozen individuals (with some likelihood of clonality) and two historical (pre-2000) collections (Fig.
AUSTRALIA. Northern Territory: 92 km W. of Dunmarra, 16°44'S, 132°10'E, 20 June 1974 (fr), P.K. Latz 5482 (DNA [DNA A0041776]); Dungowan Station, 16°44'S, 132°17'E, 10 January 1978 (fl), T.S. Henshall 1914 (DNA [DNA A0054101]); Buchanan Highway, 46.1 km E. of Top Springs, 16°43.140'S, 132°09.511'E, 22 May 2016 (fl), C.T. Martine, J.T. Cantley, L.M. Lacey & P. Jobson 4260 (DNA, BUPL); Buchanan Highway, 42.1 km E. of Top Springs, 16°42.274'S, 132°07.446'E, 30 May 2018 (fl, fr), C.T. Martine, A.J. McDonnell, J.T. Cantley, & P. Jobson 4743 (NT, DNA, BUPL); Buchanan Highway, 46.1 km E. of Top Springs, 16°43.140'S, 132°09.511'E, 30 May 2018 (fl, fr), C.T. Martine, A.J. McDonnell, J.T. Cantley, & P. Jobson 4745 (DNA, BUPL).
Couplets 3 and 4 adapted from
1 | Mature plants typically with stems 1 metre or more in height; plants possessing taproots, foliage deep green to yellow-green; occurring in the Top End region | 2 |
– | Mature plants typically with stems 1 metre or less in height (or rarely ≥ 1 m); plants rhizomatous; foliage grey to blue green to deep green; primarily occurring south of Mataranka | 5 |
2 | Foliage yellow-green to rusty-green; leaves with several shallow or deep rounded lobes; plants perennial; typically along riverbanks around southern Gulf of Carpentaria | S. melanospermum F.Muell. |
– | Foliage bright or deep green; leaves ovate to oval with none or few pointed lobes; plants biennial; mostly restricted to northern/western escarpments of the Arnhem Plateau (and Wessel Islands) | 3 |
3 | Leaves sessile; stellate hairs on upper leaf surface with lateral rays more or less porrect (held horizontally) | S. apodophyllum A.R.Bean |
– | Leaves petiolate; stellate hairs on upper leaf surface mostly with ascending lateral rays | 4 |
4 | Fruiting calyx with 2300–2700 prickles; male flowers with pedicels 3–11 mm long | S. ultraspinosum A.R.Bean |
– | Fruiting calyx with 190–310 prickles; male flowers with pedicels 11–16 mm long | S. clarkiae Symon |
5 | Erect herbs or shrubs (though branches may become lax and the plants sprawl slightly in fruiting stage) | 6 |
– | Compact to weakly erect or sprawling herbs or shrubs | 9 |
6 | Plants greater than 0.5 metre in height at maturity | S. succosum A.R.Bean & Albr. |
– | Plants 0.5 metre or less in height at maturity | 7 |
7 | Leaf blades lanceolate; lobes, if any, with sinuses less than 0.2 cm in depth | S. plastisexum Martine & McDonnell |
– | Leaf blades elliptic, ovate or rarely lanceolate; lobes frequently with sinuses ≥ 0.5 cm in depth | 8 |
8 | Leaves dissected; leaf blades ovate to oblong, 2–4 cm long, sparsely pubescent | S. diversiflorum F. Muell. |
– | Leaves deeply lobed; leaf blades ovate to elliptic, 2.5–8 cm long, densely pubescent | S. eburneum Symon |
9 | Leaves deep green; leaf blades linear, dissected, lanceolate or elliptic | 10 |
– | Leaves grey-green; leaf blades ovate | 11 |
10 | Leaf blades linear to dissected with narrow lobes or ovate to elliptic and lobed; berries globose; restricted to eastern Northern Territory, Limmen National Park region | S. jobsonii Martine, J.Cantley, & L.M.Lacey |
– | Leaf blades lanceolate to elliptic and unlobed to shallowly lobed; berries ovoid; restricted to western Northern Territory, Bullita Homestead, Judbarra National Park and vicinity | S. watneyi Martine & Frawley |
11 | Leaf margins shallowly lobed to entire, sinuate; fruit a dry berry | S. chippendalei Symon |
– | Leaf margins shallowly to deeply lobed, crenate to irregularly parted; fruit a juicy berry | 12 |
12 | Plants compact, typically much less than 0.5 m tall; restricted to north-western Northern Territory, west of Timber Creek, in the East Baines River corridor | S. eburneum Symon |
– | Plants weakly erect to sprawling, typically reaching 1 m tall; widespread in Northern Territory and western Queensland | S. succosum A.R. Bean & Albr. |
For at least five decades, the species described here has evaded easy classification by field botanists. The earliest known collections by Latz (Latz 5482, DNA) and Henshall (Henshall 1914, DNA) in the 1970s were each identified initially as S. aff. eburneum, with Solanum expert David Symon also suggesting S. aff. chippendalei for the former in an annotation (Fig.
Given this apparent ability to exhibit elements of all three possible breeding systems, we have chosen the name S. plastisexum. This name is not just a reflection of the diversity of sexual forms seen in this species, but is also a recognition that this species could prove to be a model for the sort of sexual fluidity that is present throughout the plant kingdom – where just about any sort of reproductive form one can imagine (within the constraints of genetics and development) is present (
Solanum plastisexum is a new species that serves as an example of for the diversity of sexual/reproductive form that has been increasingly recognised amongst plants – it is also evidence that attempts to recognise a “normative” sexual condition amongst the planet’s living creatures is problematic. When considering the scope of life on Earth, the notion of a constant sexual binary consisting of distinct and disconnected forms is, fundamentally, a fallacy.
This work would not have been possible without generous assistance from staff of the Northern Territory Herbaria at Palmerston (DNA) and Alice Springs (NT) and the Northern Territory Parks and Wildlife Commission. We acknowledge the members of the Australasian Virtual Herbaria (AVH) website as well as their curators and staff for their efforts in digitising and imaging specimens. We gratefully acknowledge the Traditional Owners of the lands where our collections were made. C. Moore, K. McDonnell, A. Antoine and others provided greenhouse support at Bucknell and M. Lacey provided intrepid field assistance in 2016. Dr. Nic Tippery offered advice on etymology while Dr. Nikki Young lent expertise in gender studies and language. Drs. Sandra Knapp, Franco Chiarini and Xavier Aubriot are gratefully acknowledged for their careful review and valuable comments on an earlier draft of this paper.