Research Article

Effects of nitrogen and vapour pressure deficit on

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phytomer growth and development in a C4 grass
€ ufele* and Hans Schnyder
Fang Yang, Xiao Ying Gong*, Hai Tao Liu, Rudi Scha
€t München, Alte Akademie 12, D-85354
Lehrstuhl für Grünlandlehre, Department für Pflanzenwissenschaften, Technische Universita
Freising, Germany
Received: 13 May 2016; Accepted: 19 October 2016; Published: 3 November 2016
Associate Editor: Dennis F. Whigham
€ ufele R, Schynder H. 2016. Effects of nitrogen and vapour pressure deficit on phytomer
Citation: Yang F, Gong XY, Liu HT, Scha
growth and development in a C4 grass. AoB PLANTS 8: plw075; doi:10.1093/aobpla/plw075

Abstract. Phytomers are basic morphological units of plants. Knowledge of phytomer development is essential for
understanding morphological plasticity, functional–structural modelling of plant growth and the usage of leaf charac-
teristics to indicate growth conditions at the time of production (e.g. stable isotope signals). Yet, systematic analysis on
the process of phytomer development is unavailable for wild or perennial C4 grasses. Also, effects of environmental fac-
tors, such as nitrogen nutrition or vapour pressure deficit (VPD), on coordination events of developmental processes of
C4 grasses have not been studied. This study investigates phytomer growth and development in Cleistogenes squarrosa,
a predominant C4 grass in the Eurasian steppe, grown at low (0.63 kPa) or high (1.58 kPa) VPD with low or high nitrogen
supply in controlled environments. Elongation of phytomers on marked tillers was measured daily for 13 days. Then
lengths of immature and mature phytomer components (blade, sheath and internode) of all phytomers were meas-
ured following dissection. Nitrogen nutrition and VPD had no effects on coordination of growth within and between
phytomers: phytomer tips emerged when phytomers reached 26 % of their final length, coincident with the acceler-
ation phase of its elongation; blade elongation stopped when phytomers reached 75 % of their final length and
elongation of the preceding phytomer was confined to the internode. The relationship between fraction of final phyto-
mer length and days after tip emergence for all treatments was well described by a sigmoidal function: y ¼ 1/
{1 þ exp[(1.82  x)/1.81]}. C. squarrosa exhibited little morphological plasticity at phytomer-level in response to nitrogen
supply and VPD, but a clear increase in tillering under high N supply. Also, the invariant coordination of elongation
within and between phytomers was a stable developmental feature, thus the quantitative coordination rules are ap-
plicable for predicting morphological development of C. squarrosa under contrasting levels of nitrogen nutrition or VPD.

Keywords: Coordination; developmental dynamics; elongation rate; growth duration; internode; leaf appear-
ance; leaf blade; phyllochron; plant growth model; sheath.

Introduction sheath, node, internode and axillary bud in the leaf axil
The morphology of almost all grasses can be conceptual- at the node between the leaf and the stem (Moore and
ized as a hierarchical arrangement of subunits, termed Moser 1995). Phytomer development can be described
phytomers, which are composed of a leaf blade, leaf as the succession of its components’ elongation which

* Corresponding author’s e-mail address: [email protected] or [email protected]

C The Authors 2016. Published by Oxford University Press on behalf of the Annals of Botany Company.
V
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/
licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is prop-
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 Yang et al. — Phytomer development in C. squarrosa

follows an invariable developmental sequence: the leaf elongation rate or from changes in component elong-
blade starts to elongate first, followed by the sheath and ation duration (Zhu et al. 2014), or from the timing of de-
the internode (for some species) (Fournier and Andrieu velopment events. To explicitly elucidate how plants
1998). The size, number and spatial arrangement of phy- respond to varying environments, studies performed in
tomers determine the architectural organization of indi- the field and in controlled conditions have shown that
vidual tillers (Briske 1991; Boe et al. 2000). Therefore, leaf elongation rate in grasses is very sensitive to water
knowledge of phytomer growth and development serves supply (Passioura and Gardner 1990), vapour pressure
as a basis to elucidate the rhythm of grass growth. deficit (VPD) (Ben Haj Salah and Tardieu 1996, 1997), and

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It has been repeatedly shown that the growth of phy- nutrient supply, especially of nitrogen (Volenec and
tomer components as well as the growth of successive Nelson 1983; Gastal and Nelson 1994). Nitrogen (N) defi-
phytomers is well coordinated and synchronized by cer- ciency slows leaf blade growth (Kavanova  et al. 2008),
tain events (e.g. leaf tip emergence or ligule emergence); decreases mature leaf size (Vos and van der Putten
namely, the dynamics of phytomer development are re- 1998) and reduces leaf appearance rate (Metay et al.
peated in a certain sequence along the axis of a branch 2014), but there is apparently little effect on leaf initi-
or tiller (Moore and Moser 1995; Boe et al. 2000; Boe and ation (Ma et al. 1997). It has been reported that high
Casler 2005; Forster et al. 2007). Synchrony between evaporative demand reduces maize leaf elongation rate
emergence events and the dynamics of organ extension due to water deficit (Ben Haj Salah and Tardieu 1996,
has been observed for species in which the internode 1997). Accordingly, one may propose that phytomer
does not elongate, such as C3 grasses in the vegetative growth and development in a wild grass with internode
stage (Skinner and Nelson 1995; Fournier et al. 2005), elongation in the vegetative state also responses to al-
and for species with internode elongation, such as terations of N and VPD supply. To know this phytomer
grasses during the generative (or reproductive) stages morphological plasticity in different environments is of
(Lafarge and Tardieu 2002; Zhu et al. 2014). The coordin- importance to broaden our understanding of plant life-
ation rules underlying phytomer development form an history strategies.
important basis for plant growth models in different cer- Our objectives were to investigate phytomer growth
eal crops, e.g. maize (Fournier and Andrieu 1998; Zhu and developmental characteristics of a perennial C4
et al. 2014), wheat (Evers et al. 2005; Vos et al. 2010) and grass (Cleistogenes squarrosa) and its morphological re-
barley (Buck-Sorlin et al. 2005, 2008). The need to quan- sponse to factorial combinations of nitrogen fertilization
tify the coordination of phytomer elongation, the timing and VPD treatments. C. squarrosa is a perennial C4 grass
of developmental events, growth duration, phyllochron and a co-dominant species in Inner Mongolia Grassland,
and final phytomer number is critical for crop modelling a natural arid and semiarid ecosystem (Wang and Wang
(Evers et al. 2005). Furthermore, carbon and oxygen iso- 2001; Bai et al. 2008). C. squarrosa has higher relative
tope compositions of leaf cellulose are potentially abundance in warm habitats such as sunny slopes (Gong
powerful tools for reconstruction of environmental con- et al. 2008), and it has been noted by authors that mod-
ditions, e.g. oxygen isotope composition of leaf cellulose erate to heavy grazing increased its relative abundance
reflects mainly source water isotopic signal and evapora- (Liang et al. 2002; Gong et al. 2008). Due to the domin-
tive demand (Helliker and Ehleringer 2002). Accordingly, ance in many grassland types, especially degraded
oxygen isotope composition of leaf cellulose of C. squar- grasslands, C. squarrosa is considered as a key species
rosa was shown to reflect VPD of the growth environ- for sustainable grassland and livestock management in
ment (Liu et al. 2016). For this type of studies, the this area (Liang et al. 2002). In Inner Mongolian grass-
predictability of phytomer development is essential for lands, water and nitrogen are the primary limiting factors
the dating of isotopic signals imprinted in plant material. for plant growth (Bai et al. 2008); furthermore, inter-
In addition, the knowledge of phytomer development action effects of N and water strongly influences physi-
provides important insights into environmental influ- ology and morphology of dominant species (Gong et al.
ences on plant morphological and phenotypic plasticity 2011). Moreover, soil properties exhibit strong spatial
(Boe et al. 2000). In wild (i.e. non-domesticated) or per- heterogeneity in nitrogen and other resources due to the
ennial C4 grasses phytomer development as well as the inattentively managed grazing activities, e.g. grazing in-
potential influence of environmental factors on coordin- fluences N turnover via faeces and urine redistribution
ation rules has not been studied, which impairs our (Giese et al. 2013). Thus, understanding phytomer devel-
understanding on the plasticity and predictability of mor- opment of C. squarrosa and its response to VPD and N
phological development. nutrition, has important implications for improving prod-
In principle, environmental influences on plant devel- uctivity and forage quality in this grassland. In this work,
opment can result from changes in component we hypothesized, first, that phytomer development in

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 Yang et al. — Phytomer development in C. squarrosa

C. squarrosa exhibits coordination rules similar to those with a relative humidity of 80 % and the other two with
found in other grasses, but with quantitatively different 50 % relative humidity, yielding a VPD of 0.63 kPa (V1)
dynamics in phytomer development. Second, we pre- and 1.58 kPa (V2), respectively. Thus, every combination
dicted that the growth, characterized by both leaf and of N supply and VPD (N1 V1, N1 V2, N2 V1 and N2 V2)
internode elongation, and the final length of phytomers was replicated in two growth chambers. The concentra-
are affected by N supply and VPD, mediated by the well- tion of other nutrients was kept the same in both nutri-
established effects of N and water stress on leaf elong- ent solutions: 1.0 mM MgSO4, 0.5 mM KH2PO4, 1 mM NaCl,
ation in other grasses (see above). Third, we predicted 125 mM Fe-EDTA, 46 mM H3BO3, 9 mM MnSO4, 1 mM ZnSO4,

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the constancy of coordination rules within and between 0.3 mM CuSO4 and 0.1 mM Na2MoO4.
phytomer growth across treatments. Aiming at quantita-
tive descriptions on phytomer development of C. squar- Monitoring and measurements of plant growth
rosa, we assessed phytomer elongation both for visible and calculation of phytomer elongation
growth (i.e. after emergence of the blade tip above the Sixteen plants per treatment (eight plants per growth
surrounding sheath of preceding phytomers) and invis- chamber) were tagged when the first true leaf had
ible growth (i.e. before blade tip emergence), thus cover- emerged. Ranks of leaves were counted acropetally
ing the whole elongation from (near) initiation to starting from the base of the main tiller. Accordingly, the
cessation of elongation. phytomer with the first formed leaf on the tiller, the first
tagged leaf, was referred to as phytomer 1. We started
to measure phytomer elongation on main tillers on the
Methods
24th day after the imbibition of seeds. At the start of
Plant material and growth conditions elongation measurements, the main tiller had at least
Seeds of C. squarrosa were collected in autumn 2010 ten emerged leaves. Elongation measurements lasted
and 2012 in the Xilin River watershed, China. Four seeds until the 37th day after imbibition. This corresponds to a
were sown in individual plastic tubes (5 cm diameter, thermal time of 925 degree days, close to the thermal
35 cm high) filled with quartz sand (0.3–0.8 mm diam- time of the main vegetation period for C. squarrosa in
eter). Tubes were placed in free-draining plastic boxes Inner Mongolia (Liang et al. 2002). This also ensured that
(length: 77 cm, width: 57 cm, depth: 30 cm) with 164 a sufficiently high number of phytomers completed their
tubes per box. Two boxes were placed in each of four growth during the experiment. Each day, the distance
growth chambers (Conviron PGR15, Conviron, Winnipeg, between the tip of a phytomer and the next older visible
Canada). One week after sowing, plants were thinned to ligule, and also the distance between successive visible
one plant per tube so that final density was 234 plants ligules was measured to the nearest 0.5 mm. Our prelim-
m2. Except for nutrient supply and VPD, growth condi- inary data showed that sheath elongation stopped with
tions were the same in all chambers: 16 h light period the emergence of the ligule (data not shown). Thus, phy-
with a photosynthetic photon flux density of 800 mmol tomer elongation was calculated as the change of dis-
m2 s1 at canopy height during the light period, pro- tance from phytomer tip to the next older visible ligule. A
vided by cool-white fluorescent tubes, and constant air phytomer was considered fully expanded when the dis-
temperature of 25  C throughout the light-dark cycle. tance from its tip to the next older visible ligule had
CO2 concentration in the light period was kept constant ceased to change. In most cases, tips of phytomers 12
between 380 and 390 lmol mol1. Every eight hours, a and 13 appeared (leaf tips emerged) and terminated
modified Hoagland nutrient solution (see below) was elongation during the observation period between 24
supplied by an automatic irrigation system. The nutrient and 37 d after imbibition. These data were used to calcu-
solution was completely renewed after 4 weeks, i.e. in late ‘visible growth duration’ and the visible time course
the middle of experiments. of phytomer elongation. Phytomer tip emergence was
The study had a factorial design with two treatment defined as the moment a blade tip had grown past the
factors, nitrogen supply and VPD, and each factor had highest visible ligule of the preceding phytomers.
two levels. Experiments were conducted in two separate However, as elongation measurements were performed
runs with a low and high rate of N supply. All four cham- only once a day, a phytomer tip could have emerged be-
bers were supplied with a nutrient solution containing fore our first observation on that phytomer. Therefore,
7.5 mM N (N1) in the first run, and 22.5 mM (N2) in the se- the time lag between tip emergence and our first obser-
cond run, in the form of equimolar concentrations of cal- vation on that phytomer was estimated as the distance
cium nitrate and potassium nitrate [Ca(NO3)2 and KNO3]. between the tip of the phytomer in question and the
In each experimental run, two chambers were operated next older visible ligule divided by the elongation rate

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measured just following tip emergence; and this time lag were taken into consideration excluding the shoot apex
was accounted for in the calculation of days after tip with shorter phytomers and primordia.
emergence. The phyllochron was calculated as the time
interval between the appearances of successive phyto- Assessing coordination within a phytomer and
mers. The number of tillers formed at the base of the between phytomers
shoot was also recorded. The length of successive, fully expanded phytomers (ob-
tained from destructive measurements) was used to de-
Measurements on length of phytomers and their

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termine ontogenetic changes in the final length of
components phytomers, i.e. the relationship between final phytomer
At the end of each experiment, all main tillers (16 main length and phytomer rank. By extrapolating this relation-
tillers from 16 plants per treatment) on which elongation ship, the final length of still growing phytomers (imma-
rate had been measured were sampled and dissected ture ones) was predicted. That prediction was performed
into individual phytomers. On these dissected phyto- for each individual tiller, using the data from that same
mers, the lengths of blades, sheaths and internodes tiller. The fraction of final phytomer length (fL) for imma-
were measured to the nearest 0.5 mm, and phytomer ture phytomers was calculated as:
length was obtained as the sum of the length of its com-
ponents. Thus, destructive measurements provided the fL ¼ La =LP (1)
actual length of blades, sheaths, internodes and the total
length of successive phytomers. Dissected tillers where La is the actual phytomer length at a given time,
included fully expanded phytomers, emerged (i.e. visibly Lp is predicted final phytomer length.
growing) phytomers and unemerged (invisibly growing) Accordingly, the fraction of final phytomer length is 1
phytomers whose tips had not yet emerged. A scheme of for a fully expanded phytomer. In an analogous manner,
phytomer arrangement along successive nodes on one the fractional contribution of components (blade,
tiller is presented in Fig. 1. Within a tiller, all phytomers sheath, internode) to final phytomer length was calcu-
are arranged along an axis. The basipetal succession of lated as the ratios of actual blade-, sheath- and
phytomers corresponds to a gradient of increasing phy- internode-length to predicted final phytomer length.
tomer age. Each phytomer is composed of a leaf blade, a The coordination of elongation within a phytomer was
leaf sheath, a node and an internode. Phytomer elong- assessed by plotting the fractional contribution of com-
ation starts with the (tip of the) blade and successively ponents (blade or sheath or internode) to final phytomer
passes over to elongation of the sheath and internode. length against the fractions of final phytomer length.
The sheath of a given phytomer enclosed the internode The coordination of elongation between phytomers was
of the next younger phytomer and a part of its sheath. In assessed by analysing the relationship between fractions
the dissection, only phytomers with a length >4 mm of final phytomer length of successive phytomers. The
normalized length of components and phytomers was
used to compensate for heterogeneity in plant size,
which is higher for wild plants than for genetically much
more uniform cultivars.

Constructing the time course of phytomer

development
A young phytomer grows within the sheath tube of the
preceding phytomer before tip emergence. Therefore,
the complete time course of the development of a phyto-
mer includes a visible phase (tip emergence  full expan-
Figure 1. Schematic of a mature phytomer and its components, sion) and an invisible phase (initiation  tip emergence).
and arrangement of phytomers along a tiller of C. squarrosa. The These time courses were all established by plotting the
ligule (or collar; data not shown) marks the blade-sheath junction, fraction of final phytomer length against their ages (days
and the node forms the site of insertion of the leaf on the stem. after tip emergence).
Immature, growing phytomers are situated at the tip of the tillers
The visible time course of phytomer development was
(note: for simplicity, the scheme depicts only two growing phyto-
mers, but up to five concurrently expanding phytomers in different
established using the data of phytomers (ranks 12 and
developmental stages are found along the distal part of tiller axis 13) on which the elongation rate had been monitored
upon dissection). from tip emergence to full expansion. From the

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 Yang et al. — Phytomer development in C. squarrosa

dissection of plants we obtained the final length of those data were analysed with a linear model using the gener-
phytomers, and the actual length of those phytomers on alized least squares method. This was implemented with
each day during expansion was calculated retrospect- the generalized least squares (gls) function by maximiz-
ively using the measured daily elongation rate. Thus, the ing the restricted log-likelihood (REML) method in the
fraction of final phytomer length of those phytomers ‘nlme’ package (Pinheiro et al. 2014), and the chamber
was calculated using Equation (1) (using the actual effect was also included in the model. None of the ana-
measured final length as denominator) for each day lyses yielded a significant chamber effect. For the devel-
from tip emergence to full expansion. opmental pattern of phytomers, 95 % confidence bands

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The initial phase of phytomer development was estab- of regressions were fitted using Sigmaplot (Systat
lished using the data of younger phytomers which were Software, San Jose, CA) and used to test for treatment
not fully elongated (immature) at the time of dissection. effects.
For these phytomers, their fractions of final phytomer
length were determined using Equation (1). As their ages
(the corresponding days after their tip emergence) were
Results
not known, these had to be estimated. In each tiller, an Phytomer growth and developmental parameters
immature phytomer was selected that had reached Averaged over all experiments (Table 1), the number of
60–80 % of its final length (typically the second oldest emerged (non-enclosed) phytomers that were growing
immature phytomer). Using the visible time course of simultaneously averaged 3.9 per main tiller. The average
phytomer development (see previous paragraph) the number of phytomers per main tiller observed during the
time after tip emergence of this particular phytomer was 24th–37th day after imbibition was 14. The phyllochron
estimated. This time minus the respective number of averaged 2.3 days, and the duration of visible growth
phyllochrons gave the time after tip emergence for each (i.e. the time span from tip emergence to cessation of
phytomer younger than the selected one on this tiller. elongation) was about 11 days. Mean number of tillers
We plotted the fraction of final phytomer length against was 21 and mean phytomer length was 93 mm (Fig. 2).
the calculated age of those immature phytomers to ob- In all treatments, final phytomer length decreased by
tain the initial phase of phytomer development that about 20 % between phytomer rank 8 and rank 13, the
included the invisible phase and overlapped with a small last phytomer which terminated its elongation during
range of the visible phase of phytomer development. The the observation period (Fig. 2).
construction of the initial phase of phytomer develop- Effects of VPD and N fertilizer supply or their inter-
ment was done separately for each treatment, using the actions were relatively small or non-significant, except
treatment-specific data. The visible time course and ini- for the effect of N fertilizer supply where high N increased
tial phases of phytomer development were then com- the number of tillers by 23 % relative to low N (averaged
bined to obtain the complete time course (i.e. the over VPD levels) (Table 1). Also, averaged over VPD levels,
fraction of final phytomer length vs. days before/after tip high N increased the number of phytomers per tiller by
emergence). 6 %, and shortened visible growth duration by 7 %.
Averaged over N levels, high VPD increased visible
Statistical analyses growth duration by 4 % relative to low VPD. All other par-
The effects of N supply (low and high N: N1 and N2), VPD ameters of phytomer growth and development were
(low and high VPD: V1 and V2) and their interaction on influenced by the interaction of nitrogen fertilizer supply
phytomer growth parameters were analysed by two-way and VPD. Thus, high N increased the number of visibly
analysis of variance (ANOVA) using R (R Core Team, ver- growing phytomers per tiller by 17 % and phytomer
sion 3.1.2, 2012). There were 16 replicates (16 main till- length by 8 %, and shortened the phyllochron by 13 % at
ers: eight tillers per growth chamber) in each treatment. low VPD, but not at high VPD.
For parameters that were measured on several ranks of
phytomers of a tiller, i.e. phyllochron, visible growth dur- Coordination within a phytomer
ation, maximal phytomer elongation rate and final phy- The contributions of phytomer components
tomer length, the mean value of all phytomers on that (blade, sheath and internode) to final phytomer length in
tiller was used in the statistical tests. For repeatedly expanding phytomers did not show treatment
observed parameters, e.g. the number of visibly growing effects [Fig. 3A–C; see Supporting Information—Fig. S1
phytomers, the total number of phytomers, and the for confidence intervals of the different treatments],
number of tillers, the mean values of repeated observa- so data of all treatments were pooled for further
tions on each tiller were used in the statistical tests. The analysis. Solid lines in Fig. 3A–C denote regressions with

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 Yang et al. — Phytomer development in C. squarrosa

Table 1 Growth and developmental parameters of C.squarrosa under contrasting N fertilizer and VPD treatments and the results of two-way
ANOVA for each parameter.

Parameters Treatment F value

............................................................................... .......................................................
N1 V1 N1 V2 N2 V1 N2 V2 N VPD N 3 VPD Df
......................................................................................................................................................................................................................
Number of visibly growing phytomers (tiller1) 3.6 6 0.1 3.8 6 0.1 4.2 6 0.1 3.8 6 0.1 6.083* 2.257 8.276* 58
1
Number of phytomers (tiller ) 13.4 6 0.2 13.3 6 0.2 14.5 6 0.2 13.7 6 0.2 8.073* 4.035 1.938 59

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Phyllochron (days leaf1) 2.4 6 0.1 2.4 6 0.0 2.1 6 0.0 2.4 6 0.1 8.627* 2.663 4.734* 60
Visible growth duration (days) 11.0 6 0.5 11.8 6 0.2 10.6 6 0.2 10.6 6 0.3 12.131* 4.604* 3.498 57
Number of tillers 19.7 6 1.8 17.6 6 1.0 24.0 6 1.1 21.7 6 1.6 7.754* 2.005 0.003 60

A low or high N fertilizer supply (N1 or N2) was combined with low or high VPD (V1 or V2). Values are means 6 SE (n ¼ 16). The number of vis-
ibly growing phytomers on a tiller, the number of phytomers per main tiller, and the number of tillers at the base of the plant are mean values
for the period between 24 and 37 days after imbibition; phyllochron was measured on phytomer ranks 7–16; visible growth duration, the
period from tip emergence to the cessation of elongation, was measured on ranks 12–13. Asterisk indicates significant effect (P < 0.05). Df is
the degree of freedom for the denominator in F and the degree of freedom for the numerator is 1 in all cases.

was exclusively due to blade elongation (Fig. 3A).

Transition between blade and sheath elongation was a
relatively sudden event. Sheathes were first measured
when phytomers had reached approx. 50 % of their final
length (Fig. 3B); moreover, initial sheath elongation was
slow. When blade length had reached 66 6 1 % (SE) of
final phytomer length, blades ceased to elongate and
rapid sheath elongation began. As the phytomer had at-
tained 75 % of its final length by that time, initial sheath
elongation must have contributed 9 % to final phytomer
length. Internode elongation started when the phytomer
had reached approx. 80 % of its final length (Fig. 3C).
Transition between sheath and internode elongation
also appeared to be a relatively sudden event, as inter-
Figure 2. Final (mature) length of phytomers along the axis of the
nodes significantly contributed to phytomer elongation
main tiller of C. squarrosa under contrasting nitrogen fertilizer and
VPD treatments. Phytomer rank was counted acropetally from the only when sheath elongation was nearly terminated.
base of the tiller. Error bars indicate SE (n ¼ 16).
Coordination between successive phytomers
2
y ¼ 0.73/{1 þ exp[(0.37 x)/0.17]} (R ¼ 0.90; residual Similar to the relationships within a phytomer, the coord-
standard error ¼ 0.06) for blade (A); y ¼ 0.46/ ination of development of successive phytomers was not
{1 þ exp[(0.94  x)/0.13]} (R2 ¼ 0.78; residual standard affected by treatments (Fig. 4; [see Supporting
error ¼ 0.07) for sheath (B); y ¼ 0.04*x – 0.0063 (R2 ¼ Information—Fig. S2 for confidence intervals of param-
0.06) for internode (C). At the time of the final sampling, eters and phytomer rank]). A sigmoidal function (solid
five phytomers, including emerged and unemerged phy- line in A) was fitted to the combined data of all treat-
tomers, were expanding simultaneously on a tiller [see ments: y ¼ 1.34/{1 þ exp[(0.91  x)/0.24]} (R2 ¼ 0.90; re-
Supporting Information—Fig. S1]. The relationship be- sidual standard error ¼ 0.1). A given phytomer (Pn þ 1)
tween the contribution of components to final phytomer did not elongate significantly until the preceding phyto-
length and fractional final phytomer length showed a mer (Pn) had reached approx. 25 % of its final length.
gradual transition between different phytomer ranks Then, Pn þ 1 elongated more slowly than Pn until Pn had
(from just after initiation of rapid expansion to near-fully reached approx. 50 % of final phytomer length. When
expanded). Hence, the phytomers of different ranks were the younger phytomer (Pn þ 1) had elongated to approx.
treated as representing one phytomer in different devel- 20 % 6 3 % (SE) of its final length, both phytomers elon-
opmental stages. Within a phytomer, initial expansion gated at nearly the same rate until Pn was near-fully

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Figure 4. Relationships between the lengths of two successive im-
mature (non-fully elongated) phytomers of C. squarrosa under con-
trasting N fertilizer and VPD treatments. The solid line was fitted to
the data of all treatments. Pn refers to any given immature phyto-
mer and Pn þ 1 to the corresponding next younger phytomer. All
data were obtained from destructive measurements. Each point
corresponds to a single measurement.

covered the complete visible phase of phytomer devel-

opment, which began with the appearance of the leaf tip
and ended with the cessation of internode elongation. In
all treatments, the visible time course of phytomer
elongation followed a sigmoidal pattern (coloured sym-
bols in Fig. 5). This relationship was nearly identical for
the four treatments [see Supporting Information—Fig.
S3 and Table S1 for confidence intervals of parameters].
The curve denotes the two-parameter sigmoidal function
for all data: y ¼ 1/{1 þ exp[(1.82 x)/1.81]} (R2 ¼ 0.96;
residual standard error ¼ 0.04). At the time of tip emer-
gence, phytomers had attained approx. 26 % of their
final lengths in all treatments. After tip emergence, phy-
tomer length increased linearly with time until reaching
Figure 3. Fractional contributions of phytomer components to the
final length of phytomers at successive stages of phytomer elong- approx. 85 % of final length, approx. 5 days after emer-
ation of C. squarrosa under contrasting N fertilizer and VPD treat- gence. Thereafter, phytomer elongation decreased, but
ments. Panel A, blade; panel B, sheath; Panel C, internode. The continued for another 6 days. The visible period of phyto-
solid lines were fitted to the data of all treatments. Stage of elong- mer elongation (defined here as 99 % of the final length)
ation is given by the fraction of final phytomer length, estimated
terminated at about 11 days after tip emergence.
as the ratio of the actual phytomer length to the predicted final
The reconstruction of the initial phase of phytomer de-
phytomer length (see ‘Material and Methods’ section). All data
were obtained from destructive measurements. Each point corres- velopment using the immature phytomers was based on
ponds to a single measurement. the notion that the difference in age between successive
phytomers corresponds to the phyllochron. Thus, data
elongated (defined here as 99 % of the final length). At on immature phytomers and phytomers which finished
that time, Pn þ 1 had reached 79 6 2 % (SE) of its final elongation during the observation period could be com-
length, which corresponded to the length at which blade bined to establish the complete time course of phytomer
growth stopped (see previous paragraph). elongation from 3.5 % of final phytomer length to cessa-
tion of elongation (Fig. 5). Data of immature phytomers
(black and white symbols in Fig. 5), for which the age had
Kinetics of a phytomer development been estimated, and data of phytomers, for which
For a small number of phytomers (mainly ranks 12 and the age had been directly measured (coloured symbols in
13), the observation period of phytomer elongation Fig. 5) fit a two-parameter sigmoidal function: y ¼ 1/

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 Yang et al. — Phytomer development in C. squarrosa

nutrition and VPD. Although plant development is highly

sensitive to environmental conditions (Moulia et al.
1999), to the best of our knowledge, growth coordination
in Gramineae has so far only been studied in relation to
temperature (most often expressed as thermal time
(Lafarge and Tardieu 2002; Fournier et al. 2005). In field
studies, where VPD inevitably varies over the growing
period, the timing of key events of phytomer develop-

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ment was fully explained by thermal time, which indi-
cates that VPD had no effect on coordination (Lafarge
and Tardieu 2002; Fournier et al. 2005).
The constancy of coordination across treatments
should be related to the regularity of trigger events. The
emergence of the blade tip is recognized as one trigger
Figure 5. Time course of the fraction of final phytomer length in C. event for coordination, although the exact signalling
squarrosa under contrasting N fertilizer and VPD treatments.
involved is not clear yet (Fournier et al. 2005; Zhu et al.
Coloured circles represent the visible phase of the time course of
phytomer development (see Materials and Methods): green circles, 2014). Sheath tube length affects the development of a
N1 V1; purple circles, N1 V2; red circles, N2 V1; blue circles, N2 V2. young phytomer (Wilson and Laidlaw 1985; Casey et al.
Black and white symbols represent the initial phase of phytomer 1999), as cell production of the blade is thought to be
development based on predictions of age and the final length: regulated by the light signal received by the emerging
closed circles, N1 V1; open circles, N1 V2; closed squares, N2 V1;
blade tip. In this study, the relationship between blade
open squares, N2 V2. The curve denotes the two-parameter sig-
moidal function for all data: y ¼ 1/{1 þ exp[(1.82 x)/1.81]},
length and previous sheath length showed no treatment
(R2 ¼ 0.96, residual standard error ¼ 0.04). response [see Supporting Information—Fig. S5 and
Table S3]. Moreover, at the time of tip emergence, phyto-
{1 þ exp[(x0  x)/b]}, with y denoting the fraction of final mers had reached on average 26 % of their final length
phytomer length, x days after tip emergence, b the slope with very little variation between treatments. Hence, if N
of the curve and x0 the time when phytomer growth rate nutrition and VPD treatment do not affect the relation-
was maximum. There was no significant treatment effect ship of blade and sheath tube length, coordination rules
on the complete time course of phytomer expansion can be generalized for C. squarrosa across nitrogen and
[see Supporting Information—Fig. S4 and Table S2]. VPD treatments.
For example, phytomers reached maximal growth rate
at about 2 days after tip emergence in all treatments. Coordination of phytomer development
Starting from 3.5 % of final length, the estimated time The elongation of a phytomer of C. squarrosa followed a
until tip emergence was approx. 4 days. The phase of sigmoidal pattern similar to that found in other grasses
near-linear maximum elongation began at about 1 day like maize (Fournier and Andrieu 2000), wheat and tall
before appearance of the leaf tip when the phytomer fescue (Fournier et al. 2005). It has been shown that, for
had reached approx. 20 % of final phytomer length, and wheat and tall fescue (Fournier et al. 2005), the elong-
ended about 4.5 days after tip appearance when the ation of a leaf can be subdivided into four phases. While
phytomer had reached approx. 85 % of final length. in this study, the initial phase of phytomer elongation
These phases corresponded with the phases of blade was not captured, the acceleration phase, the quasi-
and sheath elongation (Fig. 3A and B). The last elong- linear phase and the elongation-decay phase were also
ation phase was associated with internode elongation, apparent in C. squarrosa. The transition between the ac-
which occurred at considerably lower rates (Fig. 3C). celeration phase and the quasi-linear phase occurred
1 day before the tip emergence. Thus, the first phase of
visible elongation corresponded to the quasi-linear
Discussion phase of phytomer elongation, when phytomer elong-
Our study showed little morphological plasticity of ation was still exclusively due to blade elongation.
C. squarrosa at phytomer-level in response to nitrogen Maximum elongation rates were observed at 2 days after
supply and VPD, and the main variation in morphology tip emergence, when phytomers had reached 52 % of
was observed in tillering across N levels. The coordin- their final length. This corresponded to blade elongation,
ation of growth within a phytomer and between phyto- as final blade length contributed 63 % to final phytomer
mers of C. squarrosa was virtually unaffected by N length. Although elongation rates during the visible

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 Yang et al. — Phytomer development in C. squarrosa

growth phase were continuous without a significant 1998; Tardieu et al. 2000; Kavanova  et al. 2008).
break, transition between blade and sheath growth must Although high VPD clearly increased the leaf-level tran-
have occurred suddenly, as significant sheaths were only spiration rate and decreased stomatal conductance in
observed when blades were (nearly) fully elongated as the same experiment (Gong et al. 2016), the non-
revealed also in the destructive harvest. Research on a significant VPD effects on phytomer growth parameters
variety of grass species has shown that significant inter- may be due to the non-limiting water supply in our ex-
node elongation is synchronized with the end of elong- periment, i.e. the supplementation of nutrient solution
ation of the associated sheath in maize (Hesketh et al. with a frequency of three times per day. Grass species

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1988), in sorghum (Lafarge et al. 1998) and in barley were shown to be able to adjust root hydraulic conduct-
(Kirby et al. 1994). Here, the final gradual fading out of ance in response to VPD (Ocheltree et al. 2014) to main-
phytomer elongation was mainly associated with inter- tain a high leaf water potential if water supply is
node elongation. Hence, elongation rates for the inter- sufficient. The main variation in plant morphology was
node were significantly lower than elongation rates of observed in tiller development and growth, namely, the
blade and sheath. This difference is associated with the number of tillers was significantly increased by 23 % by
activity of different meristems responsible for leaf (blade N supply. These results are in line with the findings that
plus sheath) and internode growth. whole-plant relative growth rate of C. squarrosa
Elongation of successive phytomers was also tightly increased following N addition but was not affected by
coordinated: thus, the acceleration phase of the elong- VPD (Liu et al. 2016). A positive effect of N supply on the
ation of a young phytomer commenced, when the pre- tillering of grasses is a common response (Longnecker
ceding phytomer had reached approx. 25 % of its final et al. 1993; Baethgen et al. 1995; McKenzie 1998), as N
length, i.e. when the tip of the preceding phytomer fertilizer promotes the outgrowth of axillary meristems
emerged. This may also indicate a signal transduction to produce more tillers (McSteen 2009). For barley, it has
within a tiller based on tip emergence, as some studies been shown that wild varieties exhibit a similar affinity to
discussed the regulation of shoot development by hor- N as crop cultivars (Bloom 1985). Thus, the low N treat-
monal signals (Tamas 1995; Horvath et al. 2003; Schmitz ment exerted only a moderate limitation, which did not
and Theres 2005). When a phytomer terminated elong- limit the development of individual phytomers. However,
ation, the blade of the next younger phytomer was fully the reduced phyllochron in the high N treatment might
expanded and its internode started to elongate. be responsible for the positive effect on tillering, as it in-
Due to the tight coordination in phytomer growth creases the number of axillary meristems.
across N and VPD levels, the time course of phytomer de-
velopment was describable using one single equation.
The duration of elongation from the time when the phy- Conclusions
tomer had reached 3.5 % of final length until the cessa- Our results revealed a strong coordination of elongation
tion of elongation (99 % of final length) was approx. 13 both within a phytomer and between successive phyto-
d, which corresponds to 185 degree days—approx. half mers on a tiller of C. squarrosa, a wild, perennial C4 grass.
of the thermal time necessary to complete phytomer The coordination in phytomer development was virtually
elongation in Sorghum bicolor (assuming the same base unaffected by nitrogen nutrition and VPD, which indi-
temperature of 10.8  C; Lafarge and Tardieu 2002), a C4 cates that tiller development of C. squarrosa can be cap-
annual grass and crop species. Moreover, the duration of tured using general quantitative coordination rules
the linear elongation phase was about 6 days, i.e. 85 de- across VPD or nitrogen nutrient levels. On the other
gree days in our study, which is again approx. half of that hand, a clear response in tillering to N addition was
reported for S. bicolor (Lafarge and Tardieu 2002). observed. Similarly, a field study showed that both tiller
weight and tiller density responded to N and water sup-
Effects of VPD and N supply on plant morphology ply in this grassland ecosystem (Gong et al. 2015). These
The overall effects of VPD and N supply on phytomer de- results emphasize the importance of understanding
velopment were small. N fertilization supply slightly tillering kinetics in modelling the whole shoot morpho-
increased the number of visibly growing phytomers and logical development of C. squarrosa. Tip emergence, a
phytomer length, and shortened the phyllochron at low key event, may have a crucial role in signal transduction
VPD but not at high VPD. Positive effects of nitrogen fer- to coordinate phytomer elongation. Accordingly, the
tilization and low VPD on leaf elongation are well estab- time course of phytomer development was established
lished (MacAdam et al. 1989; Gastal and Nelson 1994; using observations on visibly growing phytomers, apply-
Ben Haj Salah and Tardieu 1996; Vos and van der Putten ing a sigmoidal function. This quantitative discription of

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 Yang et al. — Phytomer development in C. squarrosa

phytomer development potentially can be used for: func- complete time courses of phytomer elongation in four
tional–structural modelling, analysing morphological treatments.
plasticity, and indicating environmental factors using Table S3. Coefficients and confidence intervals of the
leaf isotopic signals of C. squarrosa. fitted linear regressions for the relationships between
the length of a blade and the length of the preceding
sheath in four treatments.
Sources of Funding

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This research was funded by the Deutsche
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