Phylogenetic Position and Generic Limits of Arabidopsis (Brassicaceae) Based on Sequences of Nuclear Ribosomal DNA

10 Pages·2003·8 MB·English

by  Steve L O'kane

PHYLOGENETIC
POSITION
AND
GENERIC OF
LIMITS
ARABIDOPSIS
BASED ON
(BRASSICACEAE)
NUCLEAR
SEQUENCES OF
DNA
RIBOSOMAL
]
Abstract
The primal) goals of lliis study writ- to assess the generic limits and monophylv of Arabidopsis and lo investigate
i
relationship- lo related lava in the family Bra-icaccac s,., |U ,. llr ,., 1, internal Iranscribed spacer region IIS- an
< >f 1 1 - ( 1
maximum
ITS-2) of nuclear ribosomal I)\A. includmg .VMS rl>\\. uere use<l in parsimony analyses to const.,..
a- -pecie- -ugge-tcd lo lie close I'elaliws. Our linding- -iim\ dial \nd>,J< >;>s>\. ,i- traditionally recognized, is polv phv lei
i.
The genus, as recircuiii-cribed lia-cd on our result-. I) now include, -pecies previously placed In ( Jirdamiimpu, an
I
Mima
Hvlundru as well as three species of Ambis and (2) ev, hides spec.es now placed in Crucihimalaya. Hrrhiffia.
Key words: Arabidopsis. Ambis. Beringia. lirassicaceae. Cm, ihimahi\<i. f> phvlogenv. Olannmbidopsis, I'srudoa
I
abidopsis.
,.,
ma
ihalit llevuli. was lust n, ndic studies and ha> played a major role in un-
(I..
I
m
processes
onimended as a model plant for e\|)erimriil,il gc l.-t -t 1. nii llic various biological in
< 1 i
&
Mey-
neties over a half century ago (Laibach, 1943). In higher plants (see references in Somerville
recent years, many biologists worldwide have lo- erowit/. 2002). The intraspecific phylogeny of A.
Zwan
As been examined Vander
cused their research on this plant. indicated by ihaliaiut lias by et al.
Patrusky (1991). the widespread acceptance of (2000). Despite the acceptance old. lliuliana as a
I.
model model organism and the sequencing and mapping
thaliana as a nrn.iiii-in is attributed lo llic
Genome
discovery thai has one of the smallest genomes ol its nuclear genome (The Arabidopsis
il
known
chromosome number 2000; Cooke
anv flowering plant, low Initiative. et al., 1996), little is
ol a
=
(n and that its genome contains lew repetitive about the other -pecies ol \rabidopsis sensu lato,
5),
sequences and intergenic spacer l)\A. and their closest relatives.
\ stir-
ill It-
I
number
prising recent finding by Blanc et al. (2000). how- A small of molecular phylogenetic stud-
members
ever, showed that although A. thaliana has a re- ies have included a lew of Arabidopsis
DNA
0'Kane
markably small genome, much of the Heynh. sensu lato (Price et al., 1994; et
is
Koch
present in more than one copy. In addition to these al., 1996; Galloway et al, 1998; et al., 1999.
gen- 2000. 2001; Yang 1999). Ho-
short et al..
examine
eration time (four lo six weeks), a small size (dozens these studies attempted to all of the taxa
can be grown small and can easily be either currently or previously included in the ge-
in a pot),
number
grown on synthetic media (Meycrnvvitz. 1989; \1ey- mis. and they included only a small of oth-
& The
The species has been used sometimes distantly related, genera. last
erowitz Pruitt. 108,.)). er.
and ge- comprehensive taxonomic account (Sehulz, 1924),
were supported
lieldwork
-.mi. h
I!, ,u\,\
(NGS-5068-93),
(icograplue Society
lion.il
i,\
)(>: ...... (,| !u<>;;
i;..i
, :
many 50 aL MnmmenhoHW
as species have heen placed the germs. Kamni 1995; Hurka.
in et >«
1 « >
I
and. although main ol these are now placed In odi- agree with Lose'- |9(>1 and lander's 1957)
1\ li\
( ) 1 (
er genera (Al-Shehhaz et al.. 1999). their phvlo- pothesis in showing thallium to lie most closel
1.
genetic relationships remain unresolved. Monophv- related to species placed Cardaminopsis. an
in In
die genus has heen make
l> ol nol vet crilicallv ticipul inn of results puhlishcd hcie and lb
l<>
determined, and even hasie hiological names a\adahle works
iiilormalioii. lor Holistic progress.
in \v
such as chromosome numbers, generalion and needed
lime, previously pulilished die iinmciiclaliual
in
hree<ling system of the memhers of the genus, novations genus Amhidopsis (O'kane &
is for the Al
lacking. Shehhaz. 1997) and have established several nev
<; eneric delimitation is perhaps on e of the most genera to accoinmodale excluded specie- Shell
VI
|
encountered prohlems
diffi< •nil anil frequently in baz el al.. I'>99). In hurl. \rahidopsis includes onf
the systemalics of the (Al-Shehhaz. llialiana and species previously included, o
1 1.
197: Rollins, 1993), an. siiggesied he. Cardaminopsis (Jones \ke
d.'iii to in
$; -. Is i\
1 I , i 1 1 ; 1 1
Ollsllrates this problem. There has Im ;en a lack of royd. 1993a. 1993b). Species now excluded Iron
among
agreemenl nnmher
on
I.imhii miisls the of ArabidopsLs are placed Thellungit-lla L
in
<).
species that belong lo Amhidopsis ami on ihe char- Schulz (Al-Shehhaz X O'kane. 199.,). \rolorularit
&
Hedge
acters that indicate generic houmlaries Leonard (Al-Shehhaz O'kane,
ils (e.g.. 1997)
iX
J.
The &
Ball, I993;lxive, 1961; Rollins, 1993). generic lanhrdgra Al-Shehhaz O'kane (Al-Shehhaz
vS
limits of Amhidopsis have heen highly unnatural. O'kane. 1999). Crurihimalaya \I-Shehhaz
,1 al.
and there were no well-defined characters separal >limamhitlop*i\ \I-Shehhaz and
I'scndoar
t et al..
mg
Irom several closely associated genera (hut ahidopsis Al-Shehhaz (Al-Shehhaz
il et al. el al.
see our taxonomic revision hased on the results of 1999). and Beringia Price (Trice 2001)
et al. el al..
O'kane
Ihis current work. vx Al-Shehhaz. 1997; Al- Our primary objectives are lo deteriniiie the ge
& Some Am-
Shehhaz. O'kane. 2002a). mono
individual iieric limits ol a morphologically coherent,
hidopsis species have heen transferred anion-; se\ phvlelic \mhiilopsis and recoup met rohusl
to a in
An
example
other genera. which
eral A. thaliana. lerprelalion of phylogenelic neighhorhood.
is
ils t
on the hasis of Schiil/s |92 synonymy was pre- wcll-o.rrnhoraled phv logeny of group
I) h. will alloy-
I
I
viouslv placed in al least nine oilier genera, in- heller evolul ionai a inlei prelatioiis to he made ol tin
Amhis
eluding Conringia Adans.. Crucifrra L. massive amounts of data now accumulating
I... lor
I
Erysimum
H. L. krause. Ilcspvris Xasturtittm thahnnn. Workers know which species con
I... I... lo
ill
i \
R. Br., I'ilosrlla koslel.. Sisymbrium and Sten- pare lo A llialiana when making interpretations.
.,
I
.
ophragma
Celak.
mo
steps wil provide a better understanding of
1
three dillerent genera. Carduminopsis (C. A. Mey.) phologic; evolution the Brassicacea
r in
Ilavek. \iahis anil llalimo/ohos Tails* h. Schulz a family great ec onomic importance fraught
.. .if wil
I
-
problem
related an under-develop<
e to
s
flahimdohos. and separated the as being
latter
much
coarser herbs wilh ihe styles narrower than delimitation.
opposed
the as \iahidopsis. which were
fruit, h-
seen as slender herbs with ihe styles slightly uar- MviKUIvl.s \M) MKIIIODS
rower than the These alleged differences are
fruit.
not mutually exclusive, and species recognized by
him one genus can be accoim We
in easily laled in included representatives of laxa least
all (at
the other. Love (1961) and Hylander (1957) iricli- al the generic level) that are now or have heen in-
caled a relalionship with Cardaminopsis based on eluded Amhidopsis Schulz. 1921; Hedge,
in (e.g..
Hedge
natural interspecific hybridization. (196H) 1965; Jafri. 1973; Al-Shehhaz. 1988: Ball. 1993).
suggested a closer relalionshi|) between \rahidopsis Taxa shown to lie near Amhidopsis in other molec-
and \mhis and unhealed
thai the two differ onlv ular studies have also heen included (I'm e
ill el al..
He
the eotyledonary position. further suggested thai 1991; O'kane 1996; Calloway 199B).
et al.. et al.,
&
Amhidopsis
wallichii (Hook. Thorns.) Buseh as have a sampling of taxa from elsewhere the
f. in
probably represents ihe link between ihe two gen- Brassicaeeae. were
I'hv logeiielic trees initially root-
An
and
era. (1987) Jain's 1973) transfer of several ed by Clromc Intra Hook, of ihe Cleomaceae.
a
(
Amhis
species from lo \rahidopsts was probablv lamilv basal Brassicaeeae (Bodman
in- lo
• th<- et al..
fluenced by Hedge's 199*
view. J„dd 1994; Hall 2002). Included
el al.. et al..
.
W
menclatural comments, are given in Table here a single round of simple laxon adililioti. Decay \alucs
1
.
possible, plant materials were collected in the field (Bremer. 1988; Donoghue et al., 1992) were found
and dried powdered silica gel. In some eases using the AutoDecay program 1.01 ol Eriksson
in
mm
tissue was obtained from plants grown -ceds. (1098). Ch.de Significance live. 2(XX)) was imple-
I
PAIP
here fresh or duel malarial was not available, we menled in In the AutoCladeS program (T. Er-
\\
used tissue from herbarinm specimens; the se- iksson; available al hllp:/A\ w w. bcigiauska.se/iu
We
new
quence Arahis bra was obtained from dex_forskning_soft.html>). found that this
lor .sea All.
GenBank. measure of support indicates those chides thai have
(Ihlh- lluelsenbeck. 1992) based
the gl statistic
<\
on K)O.(MM) random trees and by the Permutation Tail
DNA
was
Total
&
Probability (ITP) (Faith Cranston. 1992) based on
ground pinch In
in a lid
IP*
; 200 searches randomized data (PA
heuristic
of
CTAB
(O'kane
procedure as previously described
above exeepl addition was used
as sini|)le
-
1906). Amplification of the internal tran-
et al..
and
scribed -pacei region (including ITS- 5.8S.
1 .
1TS-2) was done using the conditions given
in
O'kane )%) some ITS regions
et al. ( e\ce|)t that
(1
were amplified as a -.ingle unit Using primer ITS
I nearly samples there was no evidence of
In all
cgiaacaaggtitccgtagg
las and
:V)
(rv
among
heterogeneity individual ITS copies. Rarely,
ITS-4 (While 1990) rather than as two over-
el al..
Iwo base- were present given posilion
difleieiil at a
PCP
lapping pieces. products were purified IVom
unhealed Iwo bands on an auloradiograph or
In
is
0.8% agarose gels eoiilaiiiing \ using i/ard
'I'M'' \\
I as two clear peaks on a ehromatogram. In these
PCK
Preps (Promega). Se<piences were obtained
ei-
cases the base posilion was coded using the appio
ther manual using fmol'" l)\ Sc(|iieucing
llie \
l>
priale ambiguity code. \\c inlerprel llus rare "het-
S\s|eni (Promega) or from the automated sequencer
eroz\go~il\"' as iuconi|>lele homogetiizat ion ol llie
same
the University, of Iowa using the primers
at
ITS copies and not as evidence of hybridization; an
CenPank
as were used to amplib the product. ac-
sequence would -how much more
individual vari-
Sequences
cession nimibers are gi\en Table
in 1.
were Although
ation hybridization involved. ini-
if
of the allotetraploid Anibidopsis suecica (Fries)
analyses used Clcornc Intra as the outgroup.
tial
PCP
were oblaine.l Irom loned products as
Norrl.
< inclusion of this taxon added to the complexity of
(O'Kane
previously reported et al.. 1996).
ambiguous
sequence gaps and areas wilh
lo ii-n
. 1 1
Of Ilntn
mciits. the taxa included in this slu.K.
and
ikinck ai.k;nmkni' I'IIY].()(;knktk:
sk(.)1
maximowiczii 0. Schulz was found
nrlla (Palib.) E.
be strongly supported as the basal niosl laxon.
lo
Se(|ucnees were aligned Willi the computet pmgr.im Furlliei anaUses. iheu. used /,'. nuixinmu icii as llie
MALICN K The mnlliple alignmenl of the
2.7 (Wheeler Oladslein; available oiilgmiip. lesiilliug
at
was
transcribed spacer region (ITS) 7 Id
internal
pi
in
i i i i | i i i I i i i i
I
Sequences deposited
determined In-: base-pairs length. are in
ing the following empirically par; in
CenBank (accession numbers Table and the
internal 7. exlragap 5. leading 3. trailing 3. matrix in I),
Two
alignmenl available from the author.
3 2 3 3 3 2 2 3 3 3 2 3 0. aspr. spr. quick. full is first
keepa2. keept3. and score The of the alignment that were extremely sen-
2.
i
alignment parameters and could be
not
sitive lo
and and ending gap- improved by eye 14-139 and 461-507) were not
as gap extensions as 3. initial (1
7.
bases
as 3 (not a factor in our sequences). \losi-pai -nm used in the phv logenetic analyses. In all. .'58
1
were 79 were parsimony iminformative,
nious trees were found using PALI'* 4.01)4 (Swolford. invariant.
were considered and 253 were parsimony informative.
2000). analyses characters
In all
24
be of equal weight and gaps were coded as missing Parsimony searches yielded distinct most-
to
data. Two hundred and fifty replicates of random ad- pa sir imniou.s lives of length 031. consisleucv index
i
dition using Pilch parsimony were performed using (CI) 0.48. consistency index excluding uiiinloriiia-
Tree Bisection Keconnection (TBK), Mulpars. multi- tive characters (CIU) 0.43, retention index (HI)
= pokmoip'iisic. led as missing, and 0.7;'.. and 'sealed consisleucv index (PC) ol <)..>.).
slate
". is i.
maximum was -0.5982, which
Collapse ranches length zero. Poot- The gl statistic of the data
is
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*-
S~~-g EX i^ -'- - ~
.4i^-i.S.='J^%
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i S f
t ; = -
,
.
<
The
0.01). Permutation Tail Probability (PIP) Cruribimalava. Olimarahidopsis.
I'sradoarabid,.
-
also indicated strong signal (/' 0.005). figure lanhrdgra. \rolorularia. and Tbrllun^irlla.
m.s.
I
simonious
trees, genera in the Hrassicaceae by having short
|>eti
ten rillM.I with lew -forked ones not stcllal<
I, ill
hail's, well-defined basal rosettes at least in young
while
plaills. lo (raielv piuplc)
1. \ M li ;il in. i-| hill
1 < I I
never yellow flowers, erect to slightly ascending
viously published lor smaller taxon samples in liques at least slightly torulose. much longer than
Hrassicaceae focusing on [rabidopsis (e.g.. lhc\ arc wide and glabrous, compressed (rarcK
aL
e et al., 1994; Calloway el I99K; Koch et subterete to terete), seeds uniscriale the silique.
in
:
1999, 2(KK), 2(M)1; Vang et al.. 1999). Like and cotyledons accumbent or rarely incumbent
w
&
studies, our research indicates [rabidop- (O'Kane Al-Shehbaz.
that 1997). Habit ranges from
circumscribed
is Iradilioriull) is a highly artifi- annual to short- or long-lived perennials. Chromo-
= =
group. In fact, even the tribe Sisymhrieae. the some numbers vary from x n 5 tbaliana
in
1.
=
placement 8
litional for [rabidopsis (Seliulz, 1924, to in the remaining species except for
.v
1.
=
Al-Shehbaz.
6; 1984. |9«8). is itself artificial. suecira. which an allotelraploid 20) de-
is (2/;
ma
eonlused circumscription
of [rabidopsis. as lived from = arrnosa
limit, 10) anil
(2/i
1. 1.
&
=
Lawalree (Mummenhoff
Hurka,
(I..) (2// 10)
O'Kane
1091; el al.. 1990. and references therein).
Keys
to the species and subspecies are given
in
O'Kane
likely, the and Al-Shehbaz (1997). As circumscribed
limits of Arabidopsis "would therein be consider- here, the genera Cardaminopsis llxlandm
anil A.
widened—
ably perhaps more drawn Love
or, correctly, are united with Arahidopsis. Arabidopsis
a
is
in quite another way." Jones (1904) also indicated monophyletic genus
consisting arrnosa.
of 4. A. ce-
thal two species of Arnbis, prdemonlana Roiss. brnnensis (DC.) O'Kane Al-Shehbaz.
4. croatica
\. <*
DC.
and 4. cebvnnensis might best be included in (Schott) O'Kane & Al-Shehbaz. hallrri
(L.)
I.
K
Cardaminopsis. Thus, O'Kane 4
at least as early as 1904. tax- Al-Shehbaz. lyrutu O'Kane
(L.) \l-
c\
onomie problems were &
anticipated in Arahidopsis. Shehbaz. neglevtu (Schultes) O'Kane Al-Sheh-
1.
Hesults from our
stu.b arc sullicieiil to allow a no sequences of A. pcdcmonlaiia (Boiss.) O'Kane
«.K
revision of the taxonomy of the genus [rabidopsis. \I-Shchbaz. belong-
loo. clearly [rabidopsis
in
il.
A r
strongly supported clade (bootstrap support 97 based on morphological
relationship crhen-
/r. its to 4.
decay
index clade support 0.014: see
0, Fig. nensis.
I)
containing 4. thaliana. ihc type species of the ge- All other species previously included
in [rabi-
niis, defines the limits of a recircumscribed genus dopsis are more distantly related, especially those
Arabidopsis. As staled above, we have anticipated Himalayan species now included Criicibimalaya
in
the publication ol these results bv redefining the and the Middle Laslern and central Asian Olimar-
eireumseription of Arabidopsis (O'Kane Al-Sheh- Morphologically Cnu
abidopsis. ibimalaya
i\ differs
baz, 1997), transferring species to previously rec- from [rabidopsis has some
in thai at least stellate
il
ognized genera (Al-Shehbaz O'Kane.
|00f>. Irichomcs. whereas [rabidopsis has forked
iK
tri-
1997), and lastly by erecting several new genera chomes. Olimarabidopsis differs from Arabidopsis
in
:
for species previously included in [rabidopsis (Al- its yellow, rather than while or lavender petals, pu-
Shehbaz &
1990; Al-Shehbaz O'Kane.
et al.. 1000. bcsce.il. rather than glabrous and auric,
fruits, lale
2002a; Price et al.. 2(KH Names in bold type in rather than attenuate or petiolate cauline leaves.
).
Figure represent new genera erected species Al-Shehbaz
for et al. (1000) presented im analysis of
I
previously include,
hi [nd>i,lopsis In olhci aulhors. species formerly placed based
all in [rabidopsis.
I
and the bold letter "A" indicates species previously on the results presented here, [rabidopsis ge-
a
is
we
iiicluded in [rabidopsis. In every case have mis of cncumboreal and
circuin-norlh-teiiipcrale
made
genera inonophy lelic (sensu Hennig. 1000: species. Most species, however, are confined Ku-
to
holophyletic of Ashlock. 1971). Species previously rope. Workers conducting comparative research us-
parentheses are ihe Dera\ Index: decimal \ahie- air Claiie Si^nificani
in
<
rap ^nppuii. a rue In. " V" indicates species \ariouslv placed
5()'/f 1st I.I
i
I I
\nihi(io/>M.s named elsewhere as a result ol these anakses (see Discussion).
A
surprising result our study was the discovery
ol
Ihc sister group llialiana. as experimental of a clade of species possessing pollen with
all
iii I.. I.
organism-.. This gioup n-laliniislnp implies more than the usual three colpi (see Rolyeolpate
-i-l.'i
thai all species of Ambidopsis arc equally related clade. Fig. I). Raly nological studies (Rollins. 1979;
&
showed among some
to llialiana. Unfortunately, the sister group the Rollins Ranerjee. 1979) that
to
1.
-runs cannot he given with -.•una Ihoughl not to be closely related in the Rras-
\i,il,iili>psi>. oiilideii.
. .
.
trichotomy appears below \rabid«psis sicaceae. colpi range from four to ten. These gen-
\ (Fig.
I):
according Schulz
\rabidopsis clade H"T'<//*w/A/ I'scudoambiiiopsis" era, lo (19."i<>). are as follows:
I
vkuU^CCrucihima/aya-Olimarabidopsis" cla.le). I'lnsaria iNutl. ex Tori'. t\ \. Cray) \. Cray (tribe
Calloway sequences Fepidieae. subtribe Rhysariinae). Dilliyrca Han.
usin arginine
e| al. |I99,">). u ol
i
much and recent segregate Dimorphocarpa Rollins
decarboxylase ami smaller taxon sample its
a
llepidieae. Ibcriihuae). Hook.
specif> com throughout the family cnulidcullv I\i,hhiji,i vK llaiv.
(_'!!
I I.
(Fepidieae. Fv rocarpinae). \crisyrcnia Creciie (as
Cray) and (day
Grcgfiia A. Synlblipsis A. (Fepi-
\rabi<b>p>is. iilorlunatelv. their analysis did not
I
deae. and Watson
iap-cllinael. Lrsipirrrlla S.
include any inemliers the "Crnrihimahna ( )ia
ol 0/i-
1 1
The
beae). results presented here also suggest
marabidopsis" Koch (IW)) that
.lade. found, us-
et al.
within this "polycolpate clade" taxonomic revisions
ITS sequences
ing (and with low boolsliap
-ii|>|iorl>.
We
are needed Irsipu'iella and Plnsaria. have
in
Olimam-
Capsclla and
to !»< sister to \rabi,l»psis
K
recently united these two genera Al-Shehbaz
am
bidopsis. their analysis did include (
lull not
(FKane. 2002b). except that the auriculale-leaved
Koch
me.nl.ers of Crucibimalaya. (2001) ob-
et al.
species formerly placed h'sipirivlla are recog-
in
mulk
tained similai ic->ull- using plaslidit and un-
O'Kane
nized as a distinct genus. I'a\s,>iiiu \ Al-
t
clear sequences, work needed
\dditioiial
('.lis is to
&
Shehbaz (0'Kane Al-Shehbaz,
2002).
resolve tliis issue, hut assuming that the "Capsclla-
Future work
in the family will certainly yield fur-
I'scudoarabidopsis clade" Ambidopsis
sister to
is
appears to he a valid working hypothesis.
inorphological convergence \I-Shchbaz
et al..
(
Koch
1999; 1999) and because previous
el al.. tax-
onomy
in the family has relied heavily on mor-
fruit
phology Rollins. 1993; Al-Shehbaz. I9R1)
(e.g.. |„
the exclusion of Moral and vegetative featiiies
\|
(
Illlollull "III not to study the genus
*
I Shehbaz I'W). Molecular techniques con-
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1
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Ambidopsis
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