Annals of Botany 111: 1075– 1081, 2013
doi:10.1093/aob/mct060, available online at www.aob.oxfordjournals.org
Complete tylosis formation in a latest Permian conifer stem
Zhuo Feng1,2,*, Jun Wang2, Ronny Rößler3, Hans Kerp4 and Hai-Bo Wei1
1
Yunnan Key Laboratory for Palaeobiology, Yunnan University, Kunming 650091, PR China, 2State Key Laboratory of
Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS), Nanjing 210008, PR China,
3
Museum für Naturkunde, Moritzstraße 20, D-09111 Chemnitz, Germany and 4Forschungsstelle für Paläobotanik,
Westfälische Wilhelms-Universität Münster, Schlossplatz 9, D-48143 Münster, Germany
* For correspondence. E-mail [email protected]
Received: 6 December 2012 Revision requested: 3 January 2013 Accepted: 30 January 2013 Published electronically: 26 March 2013
† Background and Aims Our knowledge of tylosis formation is mainly based on observations of extant plants;
however, its developmental and functional significance are less well understood in fossil plants. This study,
for the first time, describes a complete tylosis formation in a fossil woody conifer and discusses its ecophysiological implications.
† Methods The permineralized stem of Shenoxylon mirabile was collected from the upper Permian
(Changhsingian) Sunjiagou Formation of Shitanjing coalfield, northern China. Samples from different portions
of the stem were prepared by using the standard thin-sectioning technique and studied in transmitted light.
† Key Results The outgrowth of ray parenchyma cells protruded into adjacent tracheids through pits initially
forming small pyriform or balloon-shaped structures, which became globular or slightly elongated when they
reached their maximum size. The tracheid luminae were gradually occluded by densely spaced tyloses. The
host tracheids are arranged in distinct concentric zones representing different growth phases of tylosis formation
within a single growth ring.
† Conclusions The extensive development of tyloses from the innermost heartwood (metaxylem) tracheids to the
outermost sapwood tracheids suggests that the plant was highly vulnerable and reacted strongly to environmental
stress. Based on the evidence available, the tyloses were probably not produced in response to wound reaction or
pathogenic infection, since evidence of wood traumatic events or fungal invasion are not recognizable. Rather,
they may represent an ecophysiological response to the constant environmental stimuli.
Key words: Shenoxylon mirabile, tylose, fossil plant, conifer wood, ecophysiological response, late Permian,
China.
IN T RO DU C T IO N
In land plants, tyloses are spheroidal protoplasmic bulges that
are generally formed when the adjacent parenchyma cells,
axial parenchyma or ray cells, protrude into the dead axial conducting cells (Esau, 1965). Tyloses usually extend through the
pits of the tracheary cells and have a variety of functions, e.g.
occlude the cell cavities blocking water movement through
them (Pearce, 1996). The process of tylosis formation is complicated, and includes numerous metabolic changes, as well as
the supply of quantities of phenolic compounds, lignin and
aromatic substances (Mauseth, 2003). Tyloses have been frequently seen in extant dicotyledonous angiosperms (Saitoh
et al., 1993), but they also could be common in other groups
of vascular plants. This is uncertain since relatively few
investigations on tylosis occurrence in other plant (nondicotyledonous) groups have been conducted. Although extensive fossil records reveal that tylosis formation commonly
existed in woody plants since at least the Carboniferous
(Scheckler and Galtier, 2003), descriptions and functional analyses of tyloses to date have been obtained almost entirely
from modern dicots (Zürcher et al., 1985).
Here we report the earliest complete developmental process of
tylosis formation in a conifer stem, Shenoxylon mirabile, from
the upper Permian (Changhsingian) Sunjiagou Formation in
the Shitanjing coalfield, Ningxia Hui Autonomous Region
of northern China. Comparisons with tylosis formation in
modern plants enable inferences on the ecophysiological role
of the well-preserved tyloses in this fossil plant. The abundance
of tyloses in the wood from the uppermost Permian suggests
instability of the environment.
M AT E R I A L S A N D M E T H O D S
The Shitanjing coalfield fossil locality is situated in the northernmost part of the Ningxia Hui Autonomous Region, northern
China (Feng et al., 2011). Tectonically, the Shitanjing coalfield is located in the western Ordos (also known as Erdos or
Erduosi) sedimentary basin at the north-western edge of the
North China Block (NCB). The area of the north-western
edge of the NCB is notably rich in well-preserved late
Palaeozoic permineralized woody tree stems.
The Sunjiagou Formation in the Shitanjing coalfield is
approx. 80 m thick, representing a river– delta –lake sedimentary succession, with several pink-coloured volcanic ash deposits in the lower portion, and a thin bed of lenticular limestone
near the top of the section. The limestone bed is widely recognized in the Sunjiagou Formation elsewhere in the NCB. The
bed yielding permineralized material is composed of coarse- to
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Feng et al. — Complete tylosis formation in a latest Permian conifer stem
medium-grained sandstone with cross-bedding, representing a
fluvial sedimentary setting (Feng et al., 2011; Feng, 2012).
The silicified stem described in this paper was formally
described as Shenoxylon mirabile Feng, Wang et Roessler
and has been suggested to be a conifer (Feng et al., 2011).
Thin sections were prepared as follows. First, the specimen
was cut through transverse, tangential and longitudinal
planes into pieces of appropriate size by using a diamond
saw. The top surfaces were sequentially polished on a grinding
wheel with carborundum grades of 240, 400 and 800 in turn.
The smooth top surface was then glued onto a glass slide
with epoxy resin, and the bottom surface was ground down
to a thickness of approx. 30 mm. Most of the thin sections
were covered with a glass cover-slip using abienic balsam.
Optical examination and photomicrographs were undertaken
using a Nikon E50i transmitted light microscope equipped
with a Nikon DXM 1200F digital camera. Composite images
were stitched together using Adobe Photoshop CS v. 8.0.
The specimen, thin sections and digital photomicrographs are
reposited in the Palaeobotanical Collections of the Yunnan Key
Laboratory for Palaeobiology, Yunnan University, PR China,
with catalogue number YKLP20005.
RES ULT S
The specimen of Shenoxylon mirabile that contains the tyloses
is described here. It is approx. 150 mm in diameter, and displays a well-preserved eustele and secondary xylem. Tyloses
are recognizable throughout the primary and secondary
xylem. All tyloses are three-dimensionally preserved within
the tracheids.
In the secondary xylem, tylose-filled tracheids occur in distinct concentric zones within single growth rings. The zones of
tylose-free tracheids appear much brighter in transmitted light
than the intercalated tracheid zones that are densely filled with
tyloses (Fig. 1A, arrows). Sometimes the tylose-free tracheids
are irregularly present among the tylose-filled tracheids
(Fig. 1B). Within the tracheids, the tyloses usually are
densely spaced and polygonal in shape, occupying the entire
tracheid luminae (Fig. 1C). Single tyloses are also observed
in cross-sections (Fig. 1D); they show more or less rounded
outlines, with 1.5- to 2-mm-thick walls. Small pyriform structures, commonly ,10 mm in diameter, that protrude from ray
cells through the pits represent the early stage of tylosis formation (Fig. 1E). The pyriform structures then become somewhat
balloon-shaped with narrower bases, but sometimes show
irregular outlines (Fig. 1F).
Longitudinal sections of the secondary xylem show tyloses
in the tracheids in both the radial and tangential views
(Fig. 2A, B). There are different types of arrangement of
tyloses within the tracheids. Densely spaced polygonal
tyloses may occupy almost the entire width of the tracheids
(Fig. 2C), or groups of one to three tyloses are aligned in vertical files, reaching from one end of the tracheid to the other
(Fig. 2D). These two types of arrangement usually occur in
different tracheids (Fig. 2E). Isolated spheroidal to ellipsoidal
tyloses are present and are up to 27 mm wide and 38 mm long
(16 – 27 mm wide × 19– 38 mm long; n ¼ 50) (Fig. 2F). The
tyloses decrease in diameter toward the tapering tip of the tracheids (Fig. 2G, H). Uniseriate bordered pits occur singly or in
rows on the surface of radial tracheid walls (Fig. 3A, B).
Tangential sections also show that balloon-shaped tyloses possessing narrow bases (Fig. 3C). A single ray cell can protrude
into more than one tracheid (Fig. 3D, arrows); however, a
single tracheid can receive tyloses from more than one ray
cell (Fig. 3E). Ray cells and tylosis initials commonly
contain amorphous black substances (Fig. 3F). Tyloses are
also present in the primary xylem tracheids (Fig. 3G, H,
arrows).
The dimension and shape of the ray cells that produce tylose
are no different from the non-tylose-producing ray cells.
D IS C US S IO N
A conspicuous feature of our conifer wood is the highly developed tyloses in the tracheids through the primary to the secondary xylem. Tyloses have been documented from diverse
fossil plant groups, including progymnosperm (Scheckler and
Galtier, 2003), ferns (Williamson, 1877, 1880; Weiss, 1906;
Phillips and Galtier, 2005, 2011) and angiosperms (Bancroft,
1935; Spackman, 1948; Brett, 1960; Manchester, 1983;
Nishida et al., 1990; Poole and Francis, 1999; Privé-Gill
et al., 1999; Meijer, 2000; Poole and Cantrill, 2001; Terada
et al., 2006; Nishida et al., 2006; Castañeda-Posadas et al.,
2009). Except for some sporadic records of tylosoid occlusions
in the resin canals of fossil conifers (Jeffrey, 1904; Holden,
1915; Ogura, 1944, 1960; Nishida et al., 1977; Robison,
1977; Nishida and Oishi, 1982), there are relatively few
reports concerning tyloses in fossil conifers. A complete developmental study on tylosis formation in Palaeozoic conifers
has not been reported to date.
The first report of tylose structure in fossil conifers is of
Pityoxylon succinifer, preserved in Oligocene Baltic amber
(Conwentz, 1889). Although the classification of this wood is
still debated, and it has been assigned to Pinites (Göppert,
1841) and Pinus (Conwentz, 1889). The occlusions in the tracheids are widely accepted as being tyloses (Seward, 1919,
p. 230; Ogura, 1960). Tyloses were also noted in the Jurassic
conifer Metacedroxylon scoticum from Scotland (Jordan,
1914), the Late Jurassic conifer Protocedroxyion arancarioides
from Spitzbergen (Gothan, 1910) and the Late Triassic
Araucarioxylon sp. from Vietnam (Colani, 1919); however,
these early reports of tyloses were not further discussed.
Abundant septum-like structures in the tracheids of the
Jurassic conifer wood, Xenoxylon latiporosum, have been previously interpreted as tracheid membranes by Gothan (1910)
and Shimakura (1936). Ogura (1944) suggested that these
septum structures are tyloses. Due to the co-occurrence of
both septum and spheroidal/ovoid structures in the tracheids
of X. latiporosum from Korea, Ogura (1944) speculated that
the horizontal septa could be derived from globular tyloses.
Other specimens of the same species from the Lower
Jurassic of Japan also show similar septa in the tracheids,
but they are more pyriform (Watari, 1960). Unlike those
seen in our material, the thin septae are commonly horizontal
in the tracheids of X. latiporosum. Arnold (1952) explained the
tracheid septa as bars of Sanio (crassulae), and suspected their
origin as tyloses, based on similar material from northern
America (Medlyn and Tidwell, 1975).
Feng et al. — Complete tylosis formation in a latest Permian conifer stem
1077
B
D
A
C
E
F
F I G . 1. Shenoxylon mirabile from the upper Permian Sunjiagou Formation, Shitanjing coalfield, northern China. (A–D, F) Transverse sections: (A) tylose-filled
tracheids in a concentric zonate distribution (arrows indicate the tylose-free tracheids in the middle of the image which appear brighter in transmitted light); (B)
tylose-free tracheids irregularly distributed within the zones of tylose-filled tracheids; (C) close-up of densely spaced tyloses in tracheids; (D) isolated tyloses
showing spheroidal or ellipsoidal shape; (F) a tylose sometimes shows an irregular outline. (E) Tangential longitudinal section showing a small pyriform
tylose growing out from the parenchymatous ray cell through a pit. Scale bars are as indicated on the images. Specimen and thin sections illustrated in this
paper are housed in the Palaeobotanical Collections of the Yunnan Key Laboratory for Palaeobiology, Yunnan University, with catalogue number YKLP20005.
Ogura (1960) described two new species of Araucarioxylon
with tyloses from the Triassic and Cretaceous of Japan. The
shape of the tyloses in both species varies from pyriform to
septate. Therefore, Ogura (1960) further developed his previous assumption that ray cells protrude through the pits into
the tracheids, first forming small pyriform structures, then
the pyriform structures enlarged in both directions, and eventually the septae formed by fusion of the walls of adjacent
pyriform structures. The frequent appearance of septae may
result from the high ratio of ray cells to tracheids in the
wood (Watari, 1960). In our material, the individual tyloses
are balloon-shaped, spheroidal, or sometimes slightly ovoid
with curved ends. So far, no membranous thin septa have
been observed in our material.
‘Bud’ and balloon-like structures occurring in the tracheids of
the conifer stem, Australoxylon mondii, were illustrated from the
upper Permian of the Antarctic (Weaver et al., 1997). The small
‘buds’ were interpreted as an early stage of tylosis formation
since the ray cells protruded into the tracheid lumen, and then
the ‘buds’ expanded into balloon-like structures. Both ‘buds’
and balloon-like structures in the Antarctic material are very
similar to those in our material. Due to the fact that only one
thin section shows a few tylose structures, a complete sequence
presenting the progression of tylosis formation could not be
established in the Antarctic material (Weaver et al., 1997).
Recently, tylosis formation was reported from an Early
Jurassic permineralized conifer axis from Antarctica (Harper
et al., 2012). Because of the co-occurrence with fungi in this
stem, it seems possible that the tylosis formation was a response to fungal infection of a wood rot fungus and served
to build up mechanical barriers against the advancing
hyphae. Three developmental stages have been recognized
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Feng et al. — Complete tylosis formation in a latest Permian conifer stem
A
B
C
D
E
F
G
H
F I G . 2. Shenoxylon mirabile from the upper Permian Sunjiagou Formation, Shitanjing coalfield, northern China. (A– G) Radial longitudinal sections: (A, B)
successive fields showing tracheids in the tylose-filled wood zones; (C) densely spaced tyloses in the tracheids; (D) vertically aligned tyloses in tracheids;
(E) densely spaced and vertically aligned tyloses in isolated tracheids; (F) isolated tyloses showing spheroidal or ellipsoidal shapes; (G) vertically aligned
tyloses near the end wall of tracheids which have a smaller diameter. (H) Tangential longitudinal section showing tyloses with a smaller diameter toward the
tapering ends of the tracheids. Scale bars are as indicated on the images.
based on the dimensional and morphological features of the
tyloses in the Antarctic stem. The three stages are very
similar to the early developmental levels of tylosis formation
in our material. However, at the final stage of our material,
tyloses are further developed and tightly crowded together,
whereas in the Antarctic stem, the fully developed tyloses
are still somewhat globular and apart from each other. Our material is very well preserved with great detail but no fungal
hyphae were observed in our specimen. Therefore, we can
exclude the possibility that the prominent tyloses in our material have been induced by fungal invasion or fungal infection.
It is worth mentioning that in the progymnosperm
Protopitys buchiana from the lower Carboniferous of France
(Scheckler and Galtier, 2003), the polygonal tyloses densely
crowded in the tracheid luminae resemble those of the latest
stage of tylosis formation in our material. Because these
tyloses commonly occur near the growth ring boundaries,
Scheckler and Galtier (2003) suggested that the tylosis formation may be caused by the local dormancy water stress.
Periodic water shortage is a common phenomenon in many
terrestrial ecosystems. The tylose-filled tracheids in our specimen are obviously arranged in concentric zones. However,
Feng et al. — Complete tylosis formation in a latest Permian conifer stem
A
1079
B
C
D
E
F
G
H
F I G . 3. Shenoxylon mirabile from the upper Permian Sunjiagou Formation, Shitanjing coalfield, northern China. (A, B) Radial longitudinal sections of secondary xylem in the same area in different focal planes, showing bordered pits on the radial surface of tracheids (A) and the tyloses inside the tracheids (B). (C–F)
Tangential longitudinal sections of the secondary xylem: (C) single spheroidal tylose shows a narrow base; (D) single ray cell protrudes into different tracheids
(arrows); (E) multi-tyloses emerging from the ray cells through the pits into single tracheid; (F) ray cells and tylosis initials commonly contain black substances.
(G, H) Radial longitudinal sections of pith and primary and secondary xylem: (G) densely spaced tyloses (arrow) occurring in the innermost portion of the heartwood; (H) densely spaced tyloses (arrow) in the tracheids of the primary xylem. Abbreviations: PX, primary xylem; SX, secondary xylem; PTX, protoxylem;
MX, metaxylem. Scale bars are as indicated on the images.
several tylose-filled wood zones are recognized within a single
growth increment. It is possible that the tree lived in an
environment characterized by constant water stress.
Observations on tylosis formation in extant species reveal
that they may be triggered by various kinds of heterogeneity
in both abiotic and biotic stimuli, including mechanical injuries, infection by pathogenic microorganisms (Biggs, 1987;
Pearce, 1990), natural senescence (Dute et al., 1999), heartwood formation (Chattaway, 1949; Meyer, 1967; Panshin
and DeZeeuw, 1980; Parameswaran et al., 1985; Wilson and
White, 1986), frost (Cochard and Tyree, 1990) and flooding
(Davison and Tay, 1985). Although there are several assumptions and interpretations concerning tylosis formation in
response to special environmental conditions, a general explanation as to when and how tyloses are produced in response
to different chemical and physical stress factors imposed by
the environment has not yet been given (Sun et al., 2006,
2007). However, recent evidence indicates that ethylene
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Feng et al. — Complete tylosis formation in a latest Permian conifer stem
biosynthesis plays an important role in tylosis formation (Sun
et al., 2007; McElrone et al., 2010).
The development of tyloses has been regarded as a normal
physiological process marking the transformation from
sapwood to heartwood in many hardwood species (Leitch
et al., 1999). However, the tylose-filled tracheids in our material occur from the innermost heartwood through the outermost
of sapwood. Therefore, it is highly unlikely that the tylosis formation in our specimen would be a response to heartwood
formation.
Murmanis (1975) cut samples from Quercus rubra and investigated the number of hours required for tylosis formation. In
spring it took 6 h, but during active growth in summer only
2.5 h were required. During dormancy, 1.5 months or longer
were necessary for tyloses to appear despite temperatures conducive to metabolism. The frequent tylosis formation within a
single growth ring in our specimen might possibly indicate relatively rapid environmental changes.
Evidence for the presence of a wide variety of environmental stress factors, including sustained wind, water stress, elevated atmospheric CO2 concentration and wildfire, has been
found based on palaeobotanical data from the upper Permian
NCB (Wang and Zhang, 1998; Wang and Chen, 2001), as
well as on a global scale during this critical period (Shen
et al., 2010, 2011). According to climatic models, the NCB
was subjected to a relatively long rainfall season in its southern
part, whereas its northern part was dry (Fluteau et al., 2001).
The fossil locality of the Shitanjing coalfield is situated in
the western Ordos Basin, on the north-western edge of the
NCB. Our specimens were collected from the uppermost part
of the Sunjiagou Formation, being late Changhsingian in
age. It is therefore very compelling to invoke a relationship
between the uncommon repeated reaction of perennial
woody trees and major environmental changes. Additionally,
false rings are very commonly present in our wood, and
other woods from the same bed, also indicating severe environmental fluctuations (Feng et al., 2011; Feng, 2012).
The massive development of tyloses would effectively slow
down (or even prevent) water transport, and thus may be
viewed as a response or adaptation to the environmental
changes that were common in this terrestrial ecosystem.
Axial xylem parenchyma cells are irregularly distributed in
the fossil conifer stems, but a development of tylose from
axial parenchyma was not observed. Only the ray parenchyma
cells can account for the capacity of tylosis formation in our
material. Due to the lack of evidence of wound healing and
the repeated formation of tylose-containing wood, we believe
that tylosis formation was not induced by mechanical injury.
Conclusions
Wood is known to be a very sensitive indicator of environmental change. The anatomical particularities of our material
from northern China may provide a rare opportunity to
assess how land plants responded or adapted to environmental
changes during the late Permian.
The complete development of tylosis formation can be
observed in our conifer stem, i.e. the outgrowth of ray cells
protruding into the adjacent tracheids through the circular bordered pits and forming balloon-shaped buds, which then
became globular or slightly elongated and reach their
maximum diameter. With increasing number and size of the
tyloses, the tracheid luminae were gradually occluded.
The abundance of tyloses in our permineralized wood may
indicate that the tree was living in a time interval of extreme
ecological conditions, in which plants had to develop special
structures to adapt to the frequent changes of the environmental conditions. Repeated tylosis formation in a perennial
woody plant may indicate an adaptation of these plants to a
stressful environment. The development of false rings in the
same plant is interpreted as further indication of frequent environmental changes (Feng et al., 2011; Feng, 2012).
However, further studies of fossil woods from the same stratigraphic level in other regions are necessary to prove the significance of our current assumptions and to show the
interrelatedness of ecology, plant physiology and anatomy
some 250 million years ago.
ACK N OW L E DG E M E N T S
We would like to dedicate this paper to Prof. Herbert Süb (formerly Museum für Naturkunde Berlin) at the occasion of his
92th birthday. We thank Prof. Zhi-Yan Zhou (NIGPAS) and
Dr Michael Krings (Bavarian State Collection of
Palaeontology Munich, Germany) for their helpful comments
and insightful discussion. We thank William DiMichele and
an anonymous reviewer whose critical and detailed comments
greatly improved this paper. Financial support was partly provided by the Chinese Academy of Science Project
KZCX2-EW-120, National Basic Research Program of China
(973 Program, 2012CB821901), the National Natural Science
Foundation of China (to Z. Feng and J. Wang) and the
Volkswagen Foundation (Az.: I/84638).
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