ISSN 20790864, Biology Bulletin Reviews, 2014, Vol. 4, No. 6, pp. 496–506. © Pleiades Publishing, Ltd., 2014.

Original Russian Text © O.A. Novozhilova, L.P. Arefyeva, Yu.M. Barabasheva, E.V. Mishanova, V.F. Semikhov, 2014, published in Uspekhi Sovremennoi Biologii, 2014, Vol. 134,
No. 2, pp. 169–180.

Biochemical Specialization and Evolution

in the Triticeae Dum. Tribe (Poaceae)
O. A. Novozhilovaa, L. P. Arefyevaa, Yu. M. Barabashevab, E. V. Mishanovaa, and V. F. Semikhova
a
Tsitsin Main Botanical Garden, Russian Academy of Sciences, ul. Botanicheskaya 4, Moscow, 127276 Russia
b
Faculty of Biology, Moscow State University, Moscow, 119991 Russia
email: chemosyst@list.ru

Abstract—The problems of evolution and specialization of the tribe Triticeae are considered from the stand
point of the evolution of a seed protein complex and amino acid composition. The potential for using bio
chemical indices for the assessment of advances in the evolution and specialization of grasses are discussed.
The degree of specialization was assessed for 98 taxa of the tribe Triticeae using the index of remoteness from
a hypothetic ancestor of grasses (IR). Within the Poaceae family, Triticeae is shown to be a tribe with an
extremely high level of specialization. Henrardia and Leymus are distinguished as the most specialized genera
in the tribe. Species and genera of the tribe—second diploids—were first found to be characterized by a lower
IR as compared to donors of simple genomes. This fact is interpreted as a reflection of the biochemical despe
cialization of the taxon. The extremely low specialization of Pascopyrum smithii (IR 19.0) can be regarded as
a demonstration of the highest degree of the despecialization in tribe.

Keywords: proteins, amino acid composition, seeds, biochemical specialization, tribe Triticeae, Poaceae
DOI: 10.1134/S207908641406005X

INTRODUCTION (adapting better to new environmental conditions)

Increased economic use of cereals and the need for
ongoing breeding of cultivated species makes the
development of a natural system for Poaceae—and of
course the Triticeae tribe, as one of the most popular
tribes—especially important. Triticeae is a typical fes
tucoid tribe; the genera of this tribe are widespread
outside the tropics and in the mountainous regions of
the tropics. Many genera of Triticeae are formed via
intergeneric hybridization by combining two or more
specific genomes of other genera in one chromosome
set (Elymus, Leymus, Pascopyrum, etc.) (Tsvelev, 1987,
1991). Evolutionary secondariness of genera with
complex genomes is usually confirmed by botanical
geographic data. N.N. Tsvelev (1987) emphasized that
there is reason to believe the evolution of grasses
largely “reticulate,” and this is especially true for rep
resentatives of the Triticeae tribe. In the course of
“reticulate” evolution, despecialization of evolving
phylum occurs; the limited opportunities for further
evolution is taken as the main feature of highlyspe
cialized taxa (Tsvelev, 1975, 1991). Hybridogeneous
taxa have not only many more possibilities for gene
recombination than primary diploids, but they are also
despecialized. Many complex hybridogeneous species
have resulted from repeated hybridization. They have
unusually wide variability, which facilitates a more
rapid evolution. Species of genera with complex
genomes are more polymorphic and more active
than species of genera with simple genomes, which is
a consequence of despecialization during hybridiza
tion (Tsvelev, 1991).
The problems of evolution and the systematics and
phylogeny of the tribe and individual genera are con
stantly discussed in the scientific literature (West et al.,
1988; Frederiksen, Seberg, 1992; Yen et al., 2005,
2009; Tsvelev 2009; Kawahara, T., 2009; Zhang et al.,
2009; Tsvelev and Probatova 2010; MasonGamer
et al., 2010; Barkworth and Jacobs, et al., 2011, etc.).
However, some important aspects, such as the assess
ment of the degree of specialization of Triticeae taxa,
are understudied. The complexity of the relative spe
cialization of these taxa is determined by the “reticu
late” nature of evolution and processes of intraspecific
and intrageneric hybridization (Tsvelev, 1987, 1991).
The production of a coherent system of genera is very
difficult because of the “reticulate” nature of the evo
lution of the tribe (Tsvelev, 1991).
In the modern state of taxonomy as an integrating
discipline, the place of a taxon in the system must be
assessed from three different positions: chemosystem
atics, geneticsystematics (molecular phylogenetics),
and traditional taxonomy, correlated with the philo
sophical categories of content and internal and exter
nal forms (Semikhov 1991a, 1999). Similar positions
regarding the wide use of diverse characteristics of taxa
for the purpose of taxonomy, phylogeny and evolution

496
 BIOCHEMICAL SPECIALIZATION AND EVOLUTION
of the tribe were adopted by many researchers (Baum
et al., 1987; Seberg, 1989; Barkworth, 1992, 2009;
Monte et al., 1993; Kellogg, 2001, etc.). Regarding the
chemosystematic approach, it should be noted that
the higher the number of features is, the more objec
tive is the representation of the relationship of taxa.
This is because of the characteristics and properties of
any substance do not reflect the relationships between
taxa adequately and have only a correlative relation
with it, since the organism is much more complicated
than its constituent substrate. Second, the biochemi
cal indices used are not universal; there is an optimum
size of taxon for each class of substances, and within
this size there is the highest degree of correlation.
Comprehensive study of the characteristics and
investigation of properties of seed proteins plays an
important role in chemosystematic research. Exten
sive study of the taxa of seed plants based on seed pro
tein complex allowed the establishment of the follow
ing regularity. Phylogenetically young taxa accumulate
physiologically active low molecular weight proteins
(albumins and globulins) in seed protein complex, and
grasses accumulate prolamins. Phylogenetically
ancient taxa accumulate high molecular weight glute
lins of low solubility and proteins of nonextractable
residue, which is probably associated with the change
of energetics of the protein molecules (Blagoveshen
skii, 1966). Based on the facts described above,
Blagoveshenskii (1972) proposed index Ae for the esti
mation of quantitative characteristics of evolutionary
advancement of the taxa. Ae is the ratio of albumins,
globulins and prolamins (with high structural regular
ity) to glutelins and proteins of nonextractable residue.
The latter have lower regularity, and their organization
is close to the state of the random coil (Semikhov,
1982a, 1982b).In accordance with the hypothesis on
the direction of evolution of seed proteins (Semikhov,
1989), seed protein fractions have a common genesis.
Changes of their content in the protein complex have
directed evolutionary character, which appears by
increased organization and regularity of protein mole
cules in a series of proteins of nonextractable residue
to albumins, globulins, and prolamins. The suggestion
that the evolution of seed proteins in the tribes of
Poaceae has different rates was made based on this
hypothesis (Semikhov, 1982a, 1991b). In the seeds of
taxa considered by the majority of agrostologists as
ancient, proteins are mainly represented by two fac
tions: glutelins and proteins of nonextractable residue
(bambusoid, stipoid, panicoid tribes, etc.) (Semikhov,
1978, 1984; Semikhov et al, 1978). High levels of albu
mins, globulins, and prolamins were found in the rep
resentatives of other tribes. However, the rates of accu
mulation of these protein fractions are different in dif
ferent tribes. For example, prolamins were almost
completely absent in the seed protein complex of rep
resentatives of Brachypodieae, but the content of
albumins and globulins was high (Semikhov et al.,
1987). A high content of prolamins, accompanied
BIOLOGY BULLETIN REVIEWS Vol. 4 No. 6 2014
497
with a low concentration of albumins and globulins,
was found in representatives of the Paniceae (Semi
khov, 1984), Phalarideae (Semikhov and Kalistratova,
1977), and Poeae (Semikhov et al., 1974; Novozhilova
and Semikhov, 1981). It should be noted that prola
mins are accumulated the most rapidly. According to
Clayton (1975), the cradle of Poaceae was the rainfor
ests of the ancient supercontinent Gondwana, where
the main groups of Poaceae were formed. There is rea
son to believe that grasses did not have prolamins as a
quantitatively expressed class of proteins during the
initial stages of the family evolution. This suggestion is
confirmed by data on the exceptionally low content of
prolamins (no more than 3%) in the protein complex
of Bambusoideae and Oryzoideae subfamilies, as well
as some plants of the subfamilies of Pooideae and
Panicoideae (Semikhov, 1982b; Novozhilova et al.,
1991). Subsequent independent evolution on the con
tinents led to the appearance of different types of pro
lamins, which are closely correlated with specific cli
matic conditions (Semikhov et al., 2000a). The
appearance of prolamins in the course of the evolution
of the family and their very rapid accumulation in the
seed protein complex can be regarded as further spe
cialization of the reserve function, which increases the
adaptive capacity of Poaceae. A high content of prola
mins was found in the majority of grasses. The most
striking feature of the evolution of Poaceae seed pro
tein complex, in particular in the Triticeae tribe, is the
accumulation of prolamins. Prolamins as phylogenet
ically young specialized proteins appeared polygeneti
cally during evolution of the family as one of the phys
iological and biochemical mechanisms of adaptation
(Semikhov et al., 2006a). The special significance of
the physiological mechanisms in the evolution of
grasses was also pointed also by other authors (Clay
ton, 1975; Tsvelev, 1976). Numerous studies demon
strated that prolamins are present as a welldefined
class of proteins only in the seeds of grasses (Semikhov,
2006), while different concentrations of albumins and
globulins are present in all groups of seed plants
(Semikhov et al., 2006b). The idea that there was a dif
ferent evolutional path for the seed protein complex
led to proposal of the Is specialization index for evalu
ating biochemical specialization. This index reflects
the accumulation of specialized phylogenetically
young seed proteins—prolamins in seed protein com
plex (Semikhov, 1974). The fact that the initial less
advanced evolutionary and biochemically unspecial
ized taxa are characterized by minimal Ae and Is val
ues was demonstrated and it agrees with the agrostolo
gist estimate of antiquity of certain groups of grasses.
In addition to the evaluation of biochemical evolu
tion based on data of seed protein complex (Ae and Is
indices) in order to characterize the degree of special
ization, we used another independent index—the
index of remoteness from a hypothetic ancestor of
grasses (IR), which is based on data on the amino acid
composition of seeds. The IR index was proposed as a
498 NOVOZHILOVA et al.
result of the development of a hypothesis proposed
earlier about the amino acid composition of the hypo
thetical ancestor of grasses (Semikhov, 1988; Semi
khov et al., 2010). The formulated concept is useful for
clarification of the scope of the subfamilies and justifi
cation of the existence of this systematic category,
reflecting the most common directions of the evolu
tion of morphological and biochemical characteris
tics. The use of this concept allows us to rank genera
within tribes and subfamilies according to the degree
of biochemical specialization.
Based on the ideas and concepts discussed above,
in this study we attempted to characterize the bio
chemical aspect of specialization and evolution within
the tribe Triticeae and in comparison with other
Poaceae tribes.
MATERIALS AND METHODS
Based on the amino acid composition of seeds, we
evaluated the level of biochemical specialization of 98
species and subspecies of 21 genus of the tribe Trit
iceae. We used ideas derived from the concept of the
amino acid composition of the hypothetical ancestor
of grasses plants (Semikhov, 1988), and the distance
index was calculated based on amino acid composition
(Sokolov et al., 2007), wherein the amino acid compo
sition of each species originally was presented as a
point in a 15dimensional space (according to the
number of amino acids taken for consideration). Base
line data regarding the amino acid composition of
Triticeae representatives were given in previously pub
lished articles (Semikhov et al., 1998, 2000), where
there is reference to the sources of seeds. The index of
remoteness is considered by us to be an integral indi
cator allowing the quantifying biochemical specializa
tion of a taxon. Based on the IR value, we estimated
biochemical specialization within the tribe Triticeae
and compared it to other Poaceae tribes. The results of
research were considered in accordance with current
knowledge of tribe systematics (Watson and Dallwiz,
1994 (cited accordingly to Kawahara, 2009); Yen et
al., 2005; Barkworth, von Bothmer, 2009); the
genomes of species and genera were taken into
account (Wang et al., 1994; Genomic constitution of
taxa in Triticeae, etc.).
RESULTS AND DISCUSSION
The values of the index of remoteness from a hypo
thetical ancestor of grasses of the studied taxa of Trit
iceae are shown in the table.
Among the analyzed taxa, allooctoploid Pascopy
rum smithii (19.0), which is considerably distant from
the other species of the tribe, has an extremely low
level on the index of remoteness (which indicates the
lowest degree of biochemical specialization). The IR
values detected for Peridictyon sanctum (IR 23.6) and
the three studied Secale species (IR 23.0–24.1) were
BIOLOGY BULLETIN REVIEWS
significantly low for Triticeae. IR values not exceeding
25.0 were detected for the five species of Elymus s.1.
Three of them were from the group of species with St
and H genomes: E. alascanus, E. lanceolatus, E. mac
rourus, and two species belong to the group of StY
genomic species (E. ciliaris and E. gmelinii). A rela
tively (for the tribe) low IR level was characteristic of
representatives of Eremopyrum (27.0–29.7) and Dasy
pyrum villosum (28.8). The degree of uniformity of IR
within the genus Eremopyrum should be noted.
The highest level of biochemical specialization in
the entire Triticeae tribe was found in Henrardia per
sica (IR 40.9). Based on the IR level, representatives of
Leymus were close to Henrardia (L. arenarius and
L. mollis, IR 39.4). Very high values were consistently
obtained for all five species of Leymus, indicating a
very high degree of biochemical specialization; the IR
of the species was from 38.0 to 39.4. The genus Leymus
stands apart in the Triticeae tribe, not only based on
the very high level of IR but also on the great unifor
mity in this index. Quite high values were also obtained
for Aegilops longissima (37.5), Amblyopyrum muticum,
and Hordelymus europaeus (36.6). It should be noted
that the tribe in general is characterized by high values
of IR in the range of from 30 to 34.
Aegilops. According to the obtained characteristics,
the species are traditionally grouped in the genus
Aegilops s. l. (12 genera according to the system of
Löve, 1984 and Tsvelev, 1991) have high IR values in
the range from 28.6 (Ae. uniaristata) to 37.5 (Ae. long
issima). Most Aegilops s. l. species were in the range of
high values (30–35) and were quite close. It is interest
ing to note that species with one specific genome,
except Ae. uniaristata, had an IR value of 33.2–37.5,
which in most cases was higher than in species with
two or three specific genomes.
Elymus. For the very large genus Elymus (according
to systems of different authors, this genus includes
150–200 species) it is characterized by a high level of
IR heterogeneity, from values that are low for the tribe
(24–25) up to high values (33–34).
Eleven species were analyzed in the group of StH
genomic species Elymus s. l. (Elymus s.str. Accodingly
to Yen et al., 2005; Barkworth and von Bothmer,
2009). As noted above, significantly low IR values were
detected in three species (E. alascanus, E. lanceolatus,
E. macrourus). For another species, the values were
28.0–33.5; the average value for the group was 29.4.
StHYgenomic species (genus Campeiostachys
according to Yen et al., 2005) were characterized by
relatively high and similar IR values (32.0–33.5).
In the StYgenome species group (genus Roegneria
according to Yen et al., 2005), two species had signifi
cantly low values (24.5; 24.9), while E. pendulinus had
a high value (34.4). The group of StPYgenome spe
cies (genus Kengyilia according to Yen et al., 2005)
also was characterized by different IR values: E. batali
nii had low values for the tribe (26.5), and E. alatavicus
and E. grandiglumis had relatively high values (33.1
Vol. 4 No. 6 2014
 BIOCHEMICAL SPECIALIZATION AND EVOLUTION 499

Values of index of remoteness (IR) for taxa of the tribe Triticeae

Taxa IR Genome Taxa IR Genome
(1)
Aegilops L. E. ciliaris (Trin.) Tzvelev 24.9 StY
Ae. longissima Schweinf. & 37.5 S1 E. gmelinii (Ledeb.) Tzvelev 24.5 StY
Muschl E. pendulinus (Nevski) Tzvelev 34.4 StY
Ae. markgrafii (Greuter) Hammer 33.2 C E. glaucissimus (Popov) Tzvelev 31.1 StStY
Ae. tauschii Coss. 35.2 D E. tschimganicus (Drobov) 32.9 StStY
Ae. cylindrica Host 30.7 DC Tzvelev
Ae. comosa Sm. 35.7 M E. alatavicus (Drobov) Á. Löve 33.1 StPY
Ae.uniaristata Vis. 28.6 N E. batalinii (Krasn.) Á. Löve 26.5 StPY
Ae. ventricosa Tausch 32.8 DN E. grandiglumis (Keng) Á. Löve 33.4 StPY
Ae. crassa Boiss. 29.6 DcM E. californicus (Bolander) Gould 27.9 ND(4)
Ae. vavilovii (Zhukovsky) 31.4 DMS Eremopyrum (Ledeb.) Jaub. & F(4)
Chennaveeraiah Spach
Ae. umbellulata Zhukovsky 33.7 U E. orientale (L.) Jaub. & Spach 29.7 F
Ae. juvenalis (Thell.) Eig. 34.8 DMU E. bonaepartis (Sprengel) Nevski 28.3 F
Ae. triuncialis L. 30.4 UC E. hirsutum (Bertol.) Nevski 27.0 F
Ae. kotschyi Boiss. 33.7 SU E. triticeum (Gaertn.) Nevski 28.2 F
Ae. peregrina (Hack.) Eig. 34.6 SU; S1U Henrardia C.E. Hubbard. Q
Ae. geniculata Roth 32.3 MU H. persica (Boiss) C.E. Hubbard. 40.9 Q
Ae. lorentii Hochst. 31.5 UM Heteranthelium Hochst. Q
Agropyron J. Gaertn. P H. piliferum (Banks & Solander) 33.3 Q
A. cristatum(L.) J. Gaertner 32.2 P Hochst.
A. fragile (Roth) Candargy 30.2 P Hordelymus (Jessen) Harz Ns
A. ponticum Nevski 32.9 P H. europaeus (L.) Harz. 36.6 Ns
(5)
Amblyopyrum (Jaub. & Spach) Eig T Hordeum L.
A. muticum (Boiss) Eig. 36.6 T H. bogdanii Wilensky 30.5 H
Australopyrum (Tzvelev) Á.Löve W H. brevisubulatum Trin. 29.7 H
A. calcis Connor & Molloy 30.4 W H. chilense Roem. & Schult. 31.5 H
Crithopsis Jaub. & Spach K H. jubatum L. 32.1 H
C. delileana (Schult.) Roshev. 30.2 K H. parodii Covas 32.4 H
Dasypyrum (Coss. & Durieu) V H. procerum Nevski 35.0 H
T. Durand H. stenostachys Godron 33.2 H
D. villosum (L.) Candargy 28.8 V H. marinum (L.) Huds. 31.4 Xa
Elymus L. H. murinum L. 32.1 Xu
E. alascanus (Scribner & Merr.) 24.5 StH H. murinum ssp. glaucum 32.6
(Steud.) Tzvelev
A. Löve
E. canadensis L. 33.4 StH H. bulbosum L. 28.2 I
E. confusus (Roshev.) Tzvelev 29.7 StH(2) H. vulgare L. 31.4 I
E. caninus (L.) L. 33.5 StH H. vulgare ssp. deficiens (Steud.) 31.3 I
E. glaucus Buckl. 28.0 StH Á. Löve
E. hystrix L. 30.5 StH H. vulgare ssp. distichon (L.) 29.7 I
E. jacutensis (Drobov) Tzvelev 30.9 StH(3) Koernicke
E. lanceolatus (Scribner & Smith) 24.8 StH H. vulgare ssp. spontaneum 33.1 I
Gould (K. Koch) A. & Gr.
E. macrourus (Tutcz.) Tzvelev 24.8 StH(3) H. hexastichon L. 32.1 I
E. sibiricus L. 33.2 StH Leymus Hochst. NsXm(4,6)
E. trachycaulus (Link.) Gould ex 30.1 StH L. alaicus (Korsh.) Tzvelev 38.6 4x
Shinners L. mollis (Trin.) Pilger 39.4 4x
E. repens (L.) Gould. 27.3 StStH L. racemosus (Lam.) Tzvelev 38.0 4x
32.8 StHY L. arenarius (L.) Hochst. 39.4 8x
E. dahuricuss ssp. dahuricus L. tianschanicus (Drobov) 38.2 4x/12x
E. dahuricus ssp. excelsus (Turcz. 33.5 StHY Tzvelev
ex Griseb.) Tzvelev Pascopyrum Á. Löve StHNsXm
E. nutans Griseb. 32.4 StHY P. smithii (Rydb.) Á. Löve 19.0 StHNsXm
E. schrenkianus ssp. pamiricus 32.0 StHY Peridictyon Seberg, Fred. & Baden G(4)
(Tzvelev) Tzvelev
P. sanctum Seberg, Fred. & Baden 23.6 G
Psathyrostachys Nevski Ns

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500 NOVOZHILOVA et al.

Table. (Contd.)
Taxa IR Genome Taxa IR Genome
P. juncea (Drobov) Tzvelev 32.6 Ns T. intermedium (Host.) 29.7 EEsSt
Barkworth & D.R. Dewey
(1)
Pseudoroegneria (Nevski) A. Löve St Triticum L.
P. stipifolia (Czern. ex Nevski) A. Löve 34.3 St T. monococcum ssp. monococcum 30.1 Am
Secale L. R T. monococcum ssp. aegilopoides 32.8 Au
S. cereale L. 23.0 R (Link) A. Löve
S. montanum Guss. 24.1 R T. urartu Thum. ex Gandil. 29.9 Au
S. sylvestre Host 23.1 R T. turgidum L. 32.0 BAu
Taeniatherum Nevski Ta T. turgidum ssp. carthlicum 29.3 BAu
T. caputmedusae (L.) Nevski 32.1 Ta (Nevski) A. Löve & D. Löve
(7)
Thinopyrum T. aestivum ssp. aestivum 31.0 BAuD
T. elongatum sensu D.R. Dewey 29.0 Ec T. aestivum ssp. spelta (L.) Thell. 27.6 BAuD
T. caespitosum (Koch) Liu & Wang 30.1 EcSt T. aestivum ssp. sphaerococcum 27.9 BAuD
T. junceum L. 33.6 EbEbEc (Perc.) Mac Key
T. pungens (Pers.) A. Löve 31.9 EStStP T. tetraurartu Tum. ex Gandil. 29.6 AuAu
or EStLP
(1) Genomes in Aegilops, Triticum, Amblyopyrum; (2) Agafonov and Gerus, 2009; (3) Agafonov, 2008; (4) Liu et al., 2008; (5) Jakob and
Blattner, 2006; (6) Yen et al., 2009; (7) Genomic constitution of taxa in Triticeae (Thinopyrum); ND, not determined.

and 33.4, respectively). Octoploid E. californicus
(27.9) was the only species of Elymus that did not have
St and H genomes based on molecular data, but a
marker specific for the Ns genome, which was found
in diploid genus Psathyrostachys Nevski and in allop
loid genus Leymus Hochst., was determined. These
data allow the assumption that E. californicus does not
belong to the genus Elymus, but this assumption
requires further research (Helfgott and Mason
Gamer, 2004)
Hordeum. Representatives of the genus Hordeum
(with the H genome) (with the exception of H. brevisub
ulatum and H. bogdanii, which have low values for the
genus, and H. procerum, having the highest value) are
characterized by high IR values within a short range 31–
33. The values for the genus Hordeum with genome I,
H. marinum (genome Xa), and H. murinum (genome
Xu) were also within this range. It should be noted that
H. bulbosum (genome I) occupies an isolated position
in the group of species with genome I and in the whole
genus; it is the least specialized (IR 28.2)compared to
all other members of the genus.
Triticum. The majority of the studied representa
tives of the traditional genus Triticum (genera Crithod
ium, Gigachilon and Triticum accordingly to Löve,
1984 and Tsvelev, 1991) were characterized by high IR
values (29.3–32.8). Only hexaploid T. aestivum ssp.
spelta and T. aestivum ssp. sphaerococcum were distin
guished by significantly low IR (27.6 and 27.9, respec
tively).
Poaceae are of ancient origin, and the family was
formed no later than the end of the Cretaceous period
(Tsvelev, 1987). It is assumed that Bambusoideae is
located at the lower evolutionary level among modern
Poaceae. Another group of ancient Poaceae is
Oryzeae, which has many features in common with
bamboos. Oryzeae genera such as Zizania and Leerzia
and representatives of the genus Stipa (Stipeae) were
attributed by N.N. Tsvelev as being archaic. It should
be noted that many researchers consider these
Poaceae groups as very ancient. R.Y. Rozhevits (1946)
considered bamboos as ancient grasses close to the
hypothetical ancestor of grasses. N.P. Avdulov (1931)
considered Stipa as relict forms or forms very close to
origins of the family. I.I. Sokolova (1969) notes that
the Oryzeae tribe can be attributed to very ancient
tribes based on the number of features (the number of
stamens, complex starch grains, and small chromo
somes).
To determine the position of Triticeae in the system
of the family and to assess the level of biochemical
evolution and specialization, comparative analysis was
performed for both the taxa recognized by agrostolo
gists as being close to the hypothetical ancestor and
those more evolutionarily advanced as some festucoid
tribes (Bromeae, Poeae et al.). Representatives of
Bambusoideae and Stipeae have an extremely low
level of evolutionary advance (Ae is 0.12–0.18 and
0.05–0.16, respectively) and they do not have bio
chemical specialization, as evidenced by the
extremely low Is (0.02–0.12 and 0.01–0.04). Among
ancient Poaceae taxa, only Oryzeae have an Ae value
(0.25–0.33) that is comparable to the minimal values
for some members of the tribe Poeae, but Oryzeae are

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 BIOCHEMICAL SPECIALIZATION AND EVOLUTION
also not biochemically specialized (Is up to 0.04). In
comparison with representatives of festucoid tribes,
excluding Brachypodieae, the lack of biochemical
specialization with a low level of evolutionary
advancement can be regarded as essential support for
the position of agrostologists about the antiquity of
these groups, if we assume that the phylogenetic devel
opment moves from unspecialized to specialized.
Evaluation of the evolutionary advancement of Brac
hypodieae does not contradict with the conclusions of
N.P. Avdulov (1931) and Smith (1969), although the
Ae values were slightly higher (0.30–0.45) than for
Bambusoideae and Stipeae. However, the Is values
characterizing biochemical specialization were as low
as that of Bambusoideae and Stipeae. Representatives
of festucoid tribes are usually characterized by higher
Ae and especially Is values (Ae 0.70–4.85; Is 0.15–
0.46). Very clear differences are determined in esti
mating the degree of specialization (Is), i.e. based on
the accumulation of specialized proteins (prolamins)
in the protein complex. It should be noted that repre
sentatives of the Triticeae tribe are the most biochem
ically specialized (Is 0.29–0.54) (according to Semi
khov et al. 1983; Sokolova, 1974, 1981). If among Bro
meae some taxa (Anisantha) have Is values in the range
0.09–0.14, the Is values among Triticeae were not
below 0.29 and the maximum values were 0.47
(Lophopyrum elongatum, Aegilops ovata) and even 0.54
(Gigachylon durum).
Based on the hypothesis of the evolution of the seed
protein complex, we can assume that all of the studied
tribes contain more or less advanced taxa. Among
ancient Poaceae, the taxa (Oryzeae and Brachy
podieae) were marked; these taxa did not develop over
the course of their evolution a mechanism of bio
chemical specialization (in terms of accumulation of
prolamins), but they have relatively high values of
physiologically active, multifunctional proteins (albu
mins and globulins), which are comparable with the
highest values typical for festucoid tribes. Representa
tives of Bromeae accumulate these proteins in higher
quantities than other tribes. With respect to the bio
chemical specialization of taxa (based on Is), it should
be noted that Triticeae and Phalarideae are the most
specialized out of the studied tribes. Taxa with low Is
values were not found among representatives of these
tribes, and Phalaris minor was characterized by the
highest value of the index of specialization (Is 0.68).
A compilation of data from all of the studied taxa
shows that the most expressive trend in the evolution
of the protein complex of Poaceae is the accumulation
of prolamins, evolutionarily young highly specialized
proteins with adaptive values that, along with other
factors, allowed Poaceae to spread evenly across all
continents and all climate zones. Perhaps the process
of biochemical evolution developed toward biochemi
cal specialization, as exemplified by the tribes Trit
iceae and Phalarideae. On the contrary, in the case
where the storage mechanism of prolamines was not
BIOLOGY BULLETIN REVIEWS Vol. 4 No. 6 2014
501
sufficiently realized (Brachypodieae, some represen
tatives of Bromeae and Aveneae), the proportion of
universal physiologically active proteins increased.
The assessment of the degree of biochemical spe
cialization of taxa based on the data of the amino acid
composition of seeds (based on the index of remote
ness IR) is in good agreement with the Ae and Is
results. Ancient taxa have very low IR values. For
Bambusoideae the IR values range from 5.8 to 11.8.
The values for Stipeae (IR 3.2–6.9) and Oryzeae (IR
5.5–6.7) were in the same range. Slightly higher values
were detected for representatives of Brachypodieae
(IR 8.8–11.7). For other festucoid tribes (except Trit
iceae), the following limits of IR variation were deter
mined: Aveneae 11.0–14.8, Poeae 11.5–28.2, and
Bromeae 17.0–32.0. Thus, the festucoids are charac
terized by much higher values than the ancient group
of Poaceeae, which is interpreted by us as a higher
degree of biochemical specialization. This is consis
tent with the concepts of agrostologists that Bambuso
ideae, Stipeae, and Oryzeae are more ancient plants
compared with festucoids. At the same time, represen
tatives of Brachypodieae are biochemically specialized
to a lesser extent than Triticeae.
The obtained data of remoteness index for Triticeae
indicate a high degree of biochemical specialization of
genera of the tribe, which is in agreement with the Ae
and Is values. It should be noted that there are taxa
with different IR values in some genera of the tribe, but
in general all of the studied genera are characterized as
highly specialized, with the highest degree of bio
chemical specialization manifested in Henrardia and
Leymus. It is interesting to compare the findings of
biochemical specialization with systems based on
morphological characteristics.
Clayton and Renvoize (1986) assessed the relation
ship in the Triticeae tribe based on morphological
characters and suggested that initially there was a
divergence of the three lines of genera and genus Brac
hypodium. According to the authors, Brachypodium is
an anomalous genus in tribe. The first line of genera
was represented by following: Agropyron, Eremopyrum,
Dasypyrum, Secale, Triticum, Aegilops, Henrardia. Our
position with respect to the highest level of biochemical
specialization in the tribe Henrardia (IR 40.9) coin
cides with the vertex position of this genus in of Clayton
and Renvoize and with separate apical position in the
phylogenetic scheme of N.N. Tsvelev (1975). The tra
ditional genus Aegilops s.l., according to Clayton and
Renvoize is adjacent to Henrardia. According to our
data for the genus Aegilops s.l, the IR value is from 28.6
to 37.5, which also indicates a high but variable level of
biochemical specialization.
According to the study of the sequence of βamy
lase genes (MasonGamer, 2005), Secale was defined
as a sister group to the Dasypyrum + Triticum group.
On the diagram of tribal relationships according to
Clayton and Renvoize (1986), these three genera have
a similar location. In N.N. Tsvelev’s system (1991),
502 NOVOZHILOVA et al.
built in the order of increasing morphological special
ization (with a certain degree of conditionality), Dasy
pyrum and Secale were also closely located (positions
32, 33). Based on biochemical specialization, it can be
noted that a low level is characteristic for Secale
(23.0–24.1), and it agrees with another biochemical
specialization index Is (0.29), which is lower than that
of the other investigated representatives of Triticeae
(according to data of Semikhov et al.. 1983; Sokolova,
1974, 1981). For Dasypyrum the IR was slightly higher
(28.8) than for Secale.
The second line of genera in the tribe (according to
the system of Clayton and Renvoize) was represented
by the following: Leymus, Psathyrostachys, Hordely
mus, Hordeum, Taeniatherum, Crithopsis, and Heter
anthelium. This implies that the genus Leymus could
be the starting position for this line of genera, although
based on morphological characteristics Leymus may
be considered as a primitive genus (Tsvelev, 1975).
However, this conclusion is not consistent with the
concept of recurrence of the genus and its hybrid ori
gin (Tsvelev, 1975; Liu et al., 2008; Yen et al., 2009).
Evaluation of Leymus representatives from the stand
point of biochemical specialization (IR 38.039.4)
indicates an extremely high level of biochemical spe
cialization of the genus.
The third line of the tribe (Clayton and Renvoize,
1986) is presented by the genera Elymus, Sitanion, and
Hystrix, which in other systems belong to the same
complex genus Elymus s. l. Elymus is the most numer
ous genus of Triticeae, combining up to 200 taxa of
species rank (Tsvelev, 1991). Elymus species are widely
distributed on all continents, but the center of origin is
considered to be Central Asia, where at least half of all
known species of this genus grow. Phylogenetically
Elymus species are descended from other taxa of the
Triticeae tribe, such as Pseudoroegneria, Hordeum,
and Agropyron. According to modern concepts, the
chromosomal basis of the genus Elymus is represented
by haplomes: St, H, Y, P, W in various combinations
(Agafonov, 2004; Genomic constitution of taxa in
Triticeae). According to some authors, in accordance
with the genomic theory, the genus Elymus s.l should
be divided into several genera. For example, Roegne
ria, Kengyilia, Hystrix, etc. should be separated (Wat
son and Dallwiz, 1994 (cited accordingly to Kawa
hara, 2009); Yen et al., 2005). The level of biochemical
specialization of species Elymus s. I varies from 24.5 to
34.4. Such heterogeneity of the genus in terms of bio
chemical specialization, along with other features, is
indicative of complex evolutionary processes within
the genus.
The tree of monogenomic Triticeae groups, which
was built based on a matrix by 15 morphological char
acters (Kellogg, 1989), is rooting on Brachypodium
and Bromus, which is consistent with our positions
based on the assessment of biochemical parameters
(Ae, Is, IR). It should be noted that the location of
monogenomic genera generally coincides with a ten
BIOLOGY BULLETIN REVIEWS
dency of a gradual increase in IR values, although it
has a nonabsolute character. The group of the four
genera most closely adjacent to Brachypodium and
Bromus, (Festucopsis, Pseudoroegneria, Thinopyrum)
includes the lowspecialized (for the tribe) Peridictyon
(IR 23.6) and several more specialized representatives
of Thinopyrum. Secale (23.4) is adjacent to this group.
In the middle of the tree, including monogenomic
genera (Secale, Agropyron, Dasypyrum, Eremopyrum,
Australopyrum, Psathyrostachys, Crithopsis, Tae
niatherum, Hordeum, Heteranthelium), there is an
almost smooth increase in the index of remoteness,
from 23.4 (Secale) to 33.3 (Heteranthelium), except for
Agropyron (IR 31.8), which is located close to Secale.
The upper part of the tree is represented by Amblyopy
rum and biochemically highly specialized representa
tives of Aegilops with IR values from 35.2 to 37.5. Hen
rardia (IR 40.9) is located in the vicinity of this group
of genera.
It should be noted that one of the least developed
aspects in considering the systematics and evolution of
Triticeae concerns the possible methods of assessing
the despecialization of taxa. We have developed bio
chemical indices (IR, Is) that allow us to offer a new
and original approach to the rationale and motivation
for phenomenon of the biochemical despecialization
of taxa in the Triticeae tribe. Comparing the results
obtained by Kellogg (1989)—namely, a tree of mono
genomic groups of Triticeae and the " reticulate" rela
tionships of genera with IR data—we can assume the
following regularities. Many polyploid genera and
species have a tendency toward a decreased biochem
ical specialization in IR compared with the sources of
genomes. In our opinion this can indicate a biochem
ical despecialization of taxa that is similar to morpho
logical despecialization, which was noted by N.N.
Tsvelev (1975, 1991). This phenomenon is observed in
a number of polyploid taxa. For example, Elymus
repens (StStH) (IR 27.3) compared with Pseudoroegn
eria (St) (IR 34.3) and Hordeum (H) (IR 32.1);
Aegilops geniculata (MU) (IR 32.3) and Ae. lorentii
(UM) (31.5) compared with Ae. comosa (M) (IR 35.7)
and Ae. umbellulata (U) (IR 33.7); Ae. crassa (DM)
(IR 29.6) compared with Ae. tauschii (D) (IR 35.2)
and Ae. comosa (M) (IR 35.7); Ae. cylindrica (CD) (IR
30.7) compared with Ae. markgrafii (C) (IR 33.2) and
Ae. tauschii (D) (IR 35.2); Triticum (ABD) (IR 29.0)
compared with Triticum (AB) (30.7 IR) and Ae. taus
chii (D) (IR 35.2). An especially sharp decline was
observed in Pascopyrum smithii, the genomic constitu
tion of which is represented by four haplomes
(StHNsXm) (IR 19.0), as compared with Leymus
(NsXm) (38.7) and Elymus (a StHgenomic group of
species for which the average IR is 29.4).
In contrast to the marked tendency, an increased
level of biochemical specialization in the case of Ley
mus (NsXm) (IR 38.7) was observed. Pascopyrum
smithii has an extremely low level of biochemical spe
cialization compared with the rest of the Triticeae bio
Vol. 4 No. 6 2014
 BIOCHEMICAL SPECIALIZATION AND EVOLUTION
chemical level of specialization (IR 19.0). This iso
lated North American species, with the genomic
structure StHNsXm, 2n = 56, should be considered as
being secondary diploid (Tsvelev, 1991). N.N. Tsvelev
(1987) noted that despecialization of speciessecond
ary diploids is exhibited in morphological features that
can be attributed to the dominance of the more
ancient, and therefore usually more primitive, features
in hybrids. Based on this fact, N.N. Tsvelev (1991)
emphasizes that it is easy to make the mistake of
assigning specialized ancient genera as younger spe
cies in comparison with their despecialized descen
dants. Obviously, this conclusion may be extended to
biochemical features. Thus, based on the aforemen
tioned facts, we are inclined to regard the especially
low level of biochemical specialization of Pascopyrum
smithii, as well as the above examples of genera and
species as a secondary phenomenon, as resulting from
the phenomenon of biochemical despecialization.
In order to emphasize the relationship of the tribes
Triticeae, Brachypodieae, and Bromeae, Macfarlane
and Watson (1982) combine them into a Triticanae
supertribe. The relationship between Brachypodium
and Triticeae is well established. Clayton and Renvoize
(1986) even include Brachypodium in the Triticeae
tribe. The genera of the Brachypodieae tribe are very
similar to the genera of Triticeae (especially to Elymus)
(Tsvelev, 1987). The noncontinuous area, the nonde
termined and often significant number of flowers in
the spikelets and veins on the lower flower glumes, and
the presence of small chromosomes indicate, accord
ing to N.N. Tsvelev (1968), that Brachypodieae is the
most primitive of all three tribes. It is assumed that the
Brachypodieae tribe is a slightly modified residue of a
nowextinct Poaceae group that was the origin of the
Triticeae and Bromeae. Immunochemical studies have
shown that the Triticeae tribe is related to all festucoid
tribes (Aref’eva et al., 2011). However, neither the repre
sentatives of Brachypodieae nor Bromeae stand out
among the other tribes with respect to a higher degree of
convergence with the Triticeae, which did not support
the association of the Brachypodieae, Bromeae and Trit
iceae tribes in a Triticanae supertribe.
Bromeae occupies an intermediate position
between Triticeae and Poeae. Based on the shape of
the lodicules, the type of starch grains, and the struc
ture of the ovary, it is close to that of Triticeae but has
paniculate or racemose common inflorescences
(Tsvelev, 1987). The area of the tribe is similar to the
area of the other “festucoid” tribes of the extratropical
regions of both hemispheres and mountainous regions
of the tropics. The Bromeae tribe, as suggested by
R.Y. Rozhevits (1946), probably was isolated from
Hordeum, forming parallel lines from a common
ancestor. The results of experimental morphology and
the distribution of Bromus indicate the relative antiq
uity of this genus. At the same time, the distribution
and activity of many species indicate that this genus is
still in an active state of evolution (Stebbins, 1956).
BIOLOGY BULLETIN REVIEWS Vol. 4 No. 6 2014
503
Based on serological data, Smith (1969) suggested that
the occurrence of Bromus as an independent line of
evolution took place about the time when Triticeae
and Festuceae diverged from a common trunk. Smith
noted that they, like many of Festuceae, kept a non
specialized reproductive morphology. The genus Bro
mus and the Bromeae tribe as a whole are considered
as being primitive among festucoids (Stebbins, 1956;
Tsvelev, 1987).
Based on biochemical data, the Brachypodieae
tribe is a low biochemically specialized group, as evi
denced by its low IR values in a very narrow range
(from 8.8 to 11.7) and its Ae and Is values. In the Trit
iceae tribe even the lowest IR values (19.0 for Pascopy
rum smithii; 23.6 for Peridictyon sanctum) are much
higher than those obtained for representatives of Brac
hypodieae, including the maximal values. The fluctu
ation range of IR for the Triticeae tribe is much higher,
18.7, in comparison with 2.9 for Brachypodieae. All of
these facts, in our opinion, demonstrate intense bio
chemical evolution in the Triticeae tribe, which is
probably largely due to the “reticulate” nature of the
process. The results obtained for IR, Is, and Ae show
that even those Triticeae taxa that are the least distant
from the hypothetical ancestor are much more distant
from the original group of grasses than the most spe
cialized Brachypodieae. This conclusion is consistent
with the general ideas about the origin of Poaceae and,
in particular, the position on the relative antiquity of
the Brachypodieae tribe. Molecular data also indicate
a low rate of evolution for Brachypodium. Comparison
of the rates of evolution of Brachypodium distachyon,
representatives of Sorghum, Oryza, and Ae. tauschii
(Triticeae) showed a significantly higher rate of change
of the genome in Ae. tauschii (The international brac
hypodium initiative, 2010).
CONCLUSIONS
In our view, Triticeae is an extremely highly spe
cialized biochemically tribe. In a comparison of repre
sentatives of Triticeae with Bambusoideae, Oryzeae,
Stipeae, and Brachypodieae, it is much more special
ized. The values obtained based on the index of
remoteness are consistent with previous findings based
on the use of the coefficient of evolutionary advance
(Ae) and the index of specialization (Is). Among Poo
ideae, Triticeae is the most widespread tribe outside
the tropics and in the mountainous regions of the trop
ics. Apparently, these climatic conditions determined
the appearance of special physiological and biochem
ical adaptive mechanisms in the course of evolution,
which contributed to the formation of such highly spe
cialized tribes as Triticeae. Presumably, one such
mechanism was the appearance and accumulation of
adaptive specialized proteins—prolamins (Semikhov
et al., 2000a, 2006a). The significant content of prola
mins, as well as their extreme imbalance, resulted in a
504 NOVOZHILOVA et al.
very high degree of biochemical specialization of rep
resentatives of this tribe.
ACKNOWLEGMENTS
This work was supported by the Russian Founda
tion for Basic Research (grant no. 110400826).
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