1
Supplemental material for “Salt tolerance is evolutionarily labile in a diverse set of
2
angiosperm families”
3
4
C. Moray, X. Hua, L. Bromham
5
6
1. Composition of halophyte list
7
2. Identification of angiosperm families for taxonomic analysis
8
3. Extraction of non-monophyletic family subtrees
9
Table S1: Results of taxonomic analysis identifying families with more or fewer halophytes
10
than expected for the 146 families with one or more halophytes
11
Figure S1: Family subtrees
12
13
1. Composition of halophyte list
14
We started with a list of halophytes from Menzel and Lieth (2003), then added halophytes
15
included in lists of salt tolerant species from more recent publications. We then verified the
16
list for synonymy, as described in the Materials and Methods section. Here we outline which
17
species we included in our halophyte list from each source, since the definitions and
18
terminology used to identify salt tolerant taxa differs between sources. Because information
19
on specific levels of salinity tolerance is rare, in general we included species that were listed
20
as salt tolerant based on observational evidence (that is, reported as being able to complete
21
their life cycle under saline conditions). This means that we may have included species with
22
relatively low levels of salt tolerance, or tolerant to external and occasional exposure to
23
salinity (i.e., salt spray), so it is possible that not all species in our compiled halophyte list are
24
able to grow in highly salt-affected soil.
25
1
26
We added taxa identified as halophytes from studies in Turkey (Guvensen et al., 2006;
27
Özturk et al., 2008), China (Zhao et al., 2010), Pakistan (Khan & Qaiser, 2006). From Dagar
28
and Gurbachan (2007), we added all species listed as true halophytes, facultative halophytes
29
and glycophytes/transitional halophytes, since their definition of glycophytes/transitional
30
halophytes includes species that are able to grow in saline soils.
31
32
2. Identification of Angiosperm families for taxonomic analysis
33
We identified 411 unique families based on the APG website (Stevens, 2001), whereas some
34
sources have identified 413 (Haston et al., 2009). For this analysis we started with the 413
35
families listed by the LAPG III (Haston et al., 2009) and checked all family names against
36
the APG III website (Stevens, 2001). During this search we found that Aristolochiaceae and
37
Lactoridaceae are considered one family by the APG III website and that Buxaceae and
38
Haptanthaceae are also considered synonyms (Stevens, 2001). Here we considered these
39
families as synonyms, reducing the number of angiosperm families considered in this
40
analysis from 413 to 411. We also recognized Ripogonaceae (Haston et al., 2009) as an
41
alternative spelling of Rhipogonaceae (APG III, 2009).
42
43
3. Extraction of non-monophyletic family subtrees
44
Based on the selection criteria chosen for the phylogenetic analysis (see Methods), we needed
45
to extract some subtrees for families that were not monophyletic in the published angiosperm
46
phylogeny (Smith et al., 2011). In general we extracted all tips associated with each target
47
family, excluding a small number of tips that were either nested within clades of other
48
families or tips from other families that were nested within the clade of the target family.
49
Here we list details on each non-monophyletic family subtree, referring to specific tip
50
numbers associated with the original published phylogeny. For the Asteraceae subtree, we
2
51
excluded one Asteraceae tip that was nested within the Campanulaceae clade (tip number
52
10079). For Brassicaceae we excluded five tips that were in the Capparaceae clade (42135,
53
42136, 42145, 42168, 42171). For Euphorbiaceae we excluded four Peraceae tips that were
54
nested in the Euphorbiaceae clade (36371:36374). For Lamiaceae we excluded one tip that
55
was in the Verbanaceae clade (21536), and one Orobanchaceae (24129) that was in the
56
Lamiaceae clade. For Rosaceae we excluded one tip that was in Ranunculaceae (27875). For
57
Rubiaceae we excluded one tip that was in the Clusiaceae clade (35882).
3
Table S1: Results of taxonomic analysis identifying families with more or fewer halophytes
than expected for the 146 families with one or more halophytes. Family and order names
come from the APG III website (Stevens, 2001). Genera and species represent the mean
number of estimated genera and species in each family according to the APG III website
(Stevens, 2001). Observed number and percentage of halophytes are based on the family
affiliation of each accepted species in the halophyte list according to The Plant List (The
Plant List, 2010). For Zosteraceae there were more observed halophytes (17) than estimated
species in the family (14) since the mean species estimates come from the APG III website
and the accepted species names in the halophyte list were confirmed with The Plant List
(2010). For the analysis we considered Zosteraceae to have 100% halophytes, since the test is
not valid when there are more halophytes than total species. P-values represent whether each
family has more or fewer halophytes than expected under a binomial distribution (see
Methods).
Order name
(APG III)
Alismatales
Apiales
Arecales
Asparagales
Asterales
Brassicales
-
Family name
(APG III)
Alismataceae
Aponogetonaceae
Araceae
Butomaceae
Cymodoceaceae
Hydrocharitaceae
Juncaginaceae
Posidoniaceae
Potamogetonaceae
Ruppiaceae
Zosteraceae
Apiaceae
Araliaceae
Arecaceae
Amaryllidaceae
Asparagaceae
Iridaceae
Orchidaceae
Xanthorrhoeaceae
Asteraceae
Calyceraceae
Goodeniaceae
Bataceae
Brassicaceae
Capparaceae
Cleomaceae
Resedaceae
Species
88
43
4759
1
16
116
15
9
102
6
14
3780
1450
2361
1605
2480
2025
22075
900
23600
60
430
2
3710
480
300
75
Observed #
halophytes
3
1
4
1
15
22
3
3
6
2
14
33
3
35
15
22
10
3
3
267
1
6
2
38
10
7
5
Observed %
halophytes
3.4
2.3
0.1
100.0
93.8
19.0
20.0
33.3
5.9
33.3
100.0
0.9
0.2
1.5
0.9
0.9
0.5
0.0
0.3
1.1
1.7
1.4
100.0
1.0
2.1
2.3
6.7
p-value
fewer
0.99
0.93
0.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
0.19
0.00
0.98
0.41
0.28
0.01
0.00
0.02
0.94
0.87
0.84
1.00
0.53
0.99
0.99
1.00
p-value
more
0.06
0.36
1.00
0.01
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.85
1.00
0.02
0.68
0.79
1.00
1.00
1.00
0.07
0.46
0.29
0.00
0.54
0.03
0.04
0.00
Pattern
fewer
more
more
more
more
more
more
more
more
fewer
more
fewer
fewer
fewer
more
more
more
more
4
Order name
(APG III)
Caryophyllales
Celastrales
Ceratophyllales
Commelinales
Cornales
Cucurbitales
Dilleniales
Dipsacales
Ericales
Fabales
Fagales
Gentianales
Geraniales
Lamiales
Laurales
Liliales
Family name
(APG III)
Salvadoraceae
Aizoaceae
Amaranthaceae
Anacampserotaceae
Basellaceae
Cactaceae
Caryophyllaceae
Didiereaceae
Frankeniaceae
Gisekiaceae
Halophytaceae
Lophiocarpaceae
Molluginaceae
Nyctaginaceae
Plumbaginaceae
Polygonaceae
Portulacaceae
Sarcobataceae
Simmondsiaceae
Stegnospermataceae
Talinaceae
Tamaricaceae
Celastraceae
Ceratophyllaceae
Commelinaceae
Pontederiaceae
Loasaceae
Cucurbitaceae
Dilleniaceae
Caprifoliaceae
Ebenaceae
Ericaceae
Lecythidaceae
Primulaceae
Sapotaceae
Tetrameristaceae
Fabaceae
Polygalaceae
Surianaceae
Betulaceae
Casuarinaceae
Apocynaceae
Gentianaceae
Loganiaceae
Rubiaceae
Geraniaceae
Acanthaceae
Bignoniaceae
Lamiaceae
Linderniaceae
Orobanchaceae
Pedaliaceae
Phrymaceae
Plantaginaceae
Scrophulariaceae
Verbenaceae
Hernandiaceae
Lauraceae
Colchicaceae
Species
11
2035
2275
32
19
1866
2200
16
90
5
1
6
87
395
836
1110
70
2
1
3
27
90
1400
6
652
33
265
960
355
890
548
3995
310
2590
1100
5
19500
965
8
145
95
4555
1655
420
13150
805
4000
800
7173
195
2060
70
188
1900
1800
918
55
2500
245
Observed #
halophytes
4
45
507
1
2
11
25
2
15
1
1
1
4
9
62
40
11
1
1
1
2
55
8
1
4
3
1
14
1
2
4
1
4
14
2
1
243
3
1
1
12
43
13
1
13
1
18
9
27
2
17
1
4
34
15
15
2
2
2
Observed %
halophytes
36.4
2.2
22.3
3.1
10.5
0.6
1.1
12.5
16.7
20.0
100.0
16.7
4.6
2.3
7.4
3.6
15.7
50.0
100.0
33.3
7.4
61.1
0.6
16.7
0.6
9.1
0.4
1.5
0.3
0.2
0.7
0.0
1.3
0.5
0.2
20.0
1.2
0.3
12.5
0.7
12.6
0.9
0.8
0.2
0.1
0.1
0.5
1.1
0.4
1.0
0.8
1.4
2.1
1.8
0.8
1.6
3.6
0.1
0.8
p-value
fewer
1.00
1.00
1.00
0.96
1.00
0.03
0.73
1.00
1.00
1.00
1.00
1.00
1.00
0.99
1.00
1.00
1.00
1.00
1.00
1.00
1.00
1.00
0.05
1.00
0.20
1.00
0.24
0.92
0.12
0.01
0.33
0.00
0.78
0.01
0.00
1.00
1.00
0.01
1.00
0.56
1.00
0.31
0.20
0.07
0.00
0.00
0.00
0.69
0.00
0.67
0.21
0.84
0.95
1.00
0.24
0.97
0.98
0.00
0.54
p-value
more
0.00
0.00
0.00
0.28
0.02
0.98
0.34
0.01
0.00
0.05
0.01
0.06
0.01
0.02
0.00
0.00
0.00
0.02
0.01
0.03
0.03
0.00
0.98
0.06
0.90
0.00
0.94
0.13
0.97
1.00
0.82
1.00
0.40
1.00
1.00
0.05
0.00
1.00
0.08
0.78
0.00
0.74
0.87
0.99
1.00
1.00
1.00
0.44
1.00
0.60
0.85
0.52
0.13
0.00
0.83
0.06
0.11
1.00
0.72
Pattern
more
more
more
more
fewer
more
more
more
more
more
more
more
more
more
more
more
more
more
fewer
more
fewer
fewer
fewer
fewer
more
fewer
more
fewer
fewer
fewer
fewer
more
fewer
5
Order name
(APG III)
Magnoliales
Malpighiales
Malvales
Myrtales
Nymphaeales
Oxalidales
Pandanales
Picramniales
Piperales
Poales
Proteales
Ranunculales
Rosales
Santalales
Sapindales
Saxifragales
Solanales
Unplaced Asterid I
Vitales
Zingiberales
Family name
(APG III)
Liliaceae
Annonaceae
Bonnetiaceae
Chrysobalanaceae
Clusiaceae
Elatinaceae
Euphorbiaceae
Hypericaceae
Linaceae
Phyllanthaceae
Putranjivaceae
Rhizophoraceae
Salicaceae
Malvaceae
Neuradaceae
Thymelaeaceae
Combretaceae
Lythraceae
Melastomataceae
Myrtaceae
Onagraceae
Nymphaeaceae
Oxalidaceae
Pandanaceae
Picramniaceae
Piperaceae
Saururaceae
Bromeliaceae
Cyperaceae
Flagellariaceae
Juncaceae
Poaceae
Restionaceae
Typhaceae
Nelumbonaceae
Menispermaceae
Papaveraceae
Ranunculaceae
Elaeagnaceae
Moraceae
Rhamnaceae
Rosaceae
Ulmaceae
Olacaceae
Santalaceae
Anacardiaceae
Meliaceae
Nitrariaceae
Rutaceae
Sapindaceae
Simaroubaceae
Crassulaceae
Cynomoriaceae
Convolvulaceae
Hydroleaceae
Solanaceae
Boraginaceae
Vitaceae
Zingiberaceae
Species
610
2220
35
460
595
35
5735
560
300
1745
210
149
1010
4225
10
891
500
620
5005
4620
656
58
770
885
49
3615
6
1770
5430
4
430
11160
500
25
2
442
760
2525
45
1125
925
2520
35
57
990
873
615
16
2070
1630
110
1370
2
1625
12
2460
2755
850
1208
Observed #
halophytes
1
1
1
1
2
7
42
1
4
9
1
19
6
56
1
3
12
21
1
47
6
3
2
11
1
1
1
2
121
1
22
335
2
9
1
3
3
17
3
7
6
9
1
1
3
7
6
8
5
2
1
2
1
22
1
41
37
4
1
Observed %
halophytes
0.2
0.0
2.9
0.2
0.3
20.0
0.7
0.2
1.3
0.5
0.5
12.8
0.6
1.3
10.0
0.3
2.4
3.4
0.0
1.0
0.9
5.2
0.3
1.2
2.0
0.0
16.7
0.1
2.2
25.0
5.1
3.0
0.4
36.0
50.0
0.7
0.4
0.7
6.7
0.6
0.6
0.4
2.9
1.8
0.3
0.8
1.0
50.0
0.2
0.1
0.9
0.1
50.0
1.4
8.3
1.7
1.3
0.5
0.1
p-value
fewer
0.01
0.00
0.95
0.05
0.06
1.00
0.01
0.02
0.80
0.02
0.36
1.00
0.10
0.97
1.00
0.02
1.00
1.00
0.00
0.50
0.48
1.00
0.01
0.79
0.91
0.00
1.00
0.00
1.00
1.00
1.00
1.00
0.11
1.00
1.00
0.33
0.05
0.04
1.00
0.11
0.16
0.00
0.95
0.88
0.01
0.32
0.55
1.00
0.00
0.00
0.69
0.00
1.00
0.92
0.99
1.00
0.95
0.06
0.00
p-value
more
1.00
1.00
0.30
0.99
0.98
0.00
0.99
1.00
0.37
0.99
0.89
0.00
0.95
0.04
0.10
0.99
0.01
0.00
1.00
0.56
0.67
0.02
1.00
0.31
0.40
1.00
0.06
1.00
0.00
0.04
0.00
0.00
0.97
0.00
0.02
0.83
0.98
0.98
0.01
0.94
0.91
1.00
0.30
0.45
1.00
0.79
0.61
0.00
1.00
1.00
0.68
1.00
0.02
0.12
0.12
0.00
0.07
0.98
1.00
Pattern
fewer
fewer
fewer
more
fewer
fewer
fewer
more
more
fewer
more
more
fewer
more
fewer
fewer
fewer
more
more
more
more
more
more
fewer
fewer
more
fewer
fewer
more
fewer
fewer
fewer
more
more
fewer
6
Order name
(APG III)
Zygophyllales
Family name
(APG III)
Zygophyllaceae
Species
285
Observed #
halophytes
30
Observed % p-value
halophytes
fewer
10.5
1.00
p-value
more
0.00
Pattern
more
7
Figure S1: Family subtrees for the sample of 22 angiosperm families analysed. Origins of salt tolerance identified by maximum parsimony (see
Methods) are marked on each family with black circles. Tips in the subtrees identified as halophytes are marked in black in the ring around the
subtree.
Apiaceae
Arecaceae
●
●●
●
●
●
●
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8
Asteraceae
Goodeniaceae
●
●
●
●
●
●
●
●
●
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9
Brassicaceae
Amaranthaceae
●
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10
Tamaricaceae
Cucurbitaceae
●
●
●
●
●
●
●
●
●
11
Primulaceae
Casuarinaceae
●
●
●
●
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●
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●
●
12
Rubiaceae
Acanthaceae
●
●
●
●
●
●
●
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●
●
●
●
13
Lamiaceae
Euphorbiaceae
●
●
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●
●
●
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●
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●
14
Rhizophoraceae
Combretaceae
●
●
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●
●
●
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●
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●
●
15
Lythraceae
Myrtaceae
●
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16
Cyperaceae
Juncaceae
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17
Poaceae
Rosaceae
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18
References
Dagar, J.C. & Gurbachan, S. 2007. Biodiversity of saline and waterlogged environments:
Documentation, utilization and management. NBA Scientific Bulletin Number - 9,
National Biodiversity Authority, Chennai, Tamil Nadu, India, pp. 78.
Guvensen, A., Gork, G. & Özturk, M. 2006. An overview of the halophytes in Turkey.
Sabkha ecosystems, pp. 9–30. Springer, Netherlands.
Haston, E., Richardson, J.E., Stevens, P.F., Chase, M.W. & Harris, D.J. 2009. The Linear
Angiosperm Phylogeny Group (LAPG) III: A linear sequence of the families in APG III.
Bot. J. Linn. Soc. 161: 128–131.
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