4. Discussion
Results from this study showed that shade avoidance cues from early
emerging weeds (weeds that emerge with the sugar beet) have a more
detrimental impact on sugar beet growth and development than
late-emerging weeds. Sugar beet responded to an early shade avoidance
cue by adjusting leaf orientation (hyponasty) to optimize light
interception (Figure 3 and 4). Even when the weed was removed, the
hyponastic response remained. These responses result in a reduced number
of leaves and reduced leaf area for light capture and photosynthesis
(Figure 3), thereby reducing shoot and root biomass (Figure 6). These
results suggest a constitutive response where most, or even all, of the
season-long shade avoidance response (SAR) in sugar beet growth is fixed
by the time the sugar beet crop has reached the two true-leaf stage
(approximately 330 GDD after planting). Removing weeds after that time
had a small impact on the number of sugar beet leaves, but did not allow
recovery of leaf area or biomass production, indicating that a
constitutive shade avoidance response (CoSAR) may play a key role in
crop yield loss due to weeds.
Studies have shown that stem and petiole extension and hyponasty are
among the most common SARs (Cerrudo et al.,
2017; Franklin & Whitelam, 2005;
Yang & Li, 2017). Leaf orientation is an
important factor influencing light interception in plants. This is
because leaf angle relative to the direction of sunlight determines both
the photosynthetic performance of the leaves at the top of the canopy as
well as the amount of light available to lower leaves
(Van Zanten, Pons, Janssen, Voesenek, &
Peeters, 2010). At the canopy level, steeper leaf angles reduce mutual
shading and thus, maximize light interception
(Mullen, Weinig, & Hangarter, 2006).
Since reduced R:FR is a cue for impending competition, it is not
surprising that hyponasty is an intrinsic part of the shade avoidance
syndrome (Van Zanten et al., 2010). Sugar
beet has a rosette growth habit in the first season of growth and thus,
hyponasty appears to be the strategy for projecting leaves for optimal
light interception. We observed shade avoidance-induced hyponasty in the
form of increased leaf angles in our study (Figure 3 and 4); however,
sugar beet did not increase petiole or leaf length in response to shade
avoidance cues as might be expected. In fact, we observed a reduction in
petiole length, total leaf length, and petiole proportion of leaves in
response to season-long shade avoidance cues in our greenhouse study
(Figure 5).
Previous studies have found that reduced R:FR resulted in fewer leaves
in A. thaliana (Xie et al., 2017)
maize (Page, Liu, Cerrudo, Lee, &
Swanton, 2011), and soybean
(Green-Tracewicz, Page, & Swanton,
2012). We have previously shown that leaf number is reduced by
season-long shade avoidance cues in three different sub-species ofB. vulgaris (Schambow et al.,
2019). Here, we show that although the first two leaf pairs were least
affected with respect to leaf size and area (Figure 5), subsequent sugar
beet leaf development was reduced substantially even if weeds were
removed early in plant development (Figure 3). Compared to season-long
weed-free treatments in this study, the number of sugar beet leaves were
reduced 10% if weeds were present for the first 16 days after
emergence, and only reduced 12% if weeds were added 16 days after
emergence and remained for the next 51 days (the average time from two
true-leaf stage to harvest in this study). Early-emerging weeds have
more impact on sugar beet leaf development compared to late-emerging
weeds.
The relationship between sugar beet leaf area (Figure 3 E & F) and the
duration of weed presence follows a similar trend as number of leaves,
with early presence of the shade avoidance cue initiating an
irreversible season-long response. Since leaf area is a function of leaf
size and number, it appears the reduction in sugar beet leaf area was at
least partly due to reduced number of leaves. Results from the
greenhouse study showed that, in addition to reduced number of leaves,
reflected FR light reduced sugar beet leaf width, petiole length, and
total leaf length as well (Figure 5). Differences in sugar beet leaf
size were most pronounced after the first six true-leaves had appeared,
which corresponds to the transition from leaf canopy-dominated growth to
root cambium development (followed by storage root and sugar
accumulation dominated phase) (Milford,
2006). Most capacity for storage root size and weight is laid down by
the sixth true leaf stage (Milford,
2006).
Although increased petiole elongation is a common response to shade
avoidance cues (Weijschedé, Martínková, De
Kroon, & Huber, 2006), we observed a reduction in petiole length
(Figure 5C), even as a proportion of total leaf length (Figure 5E), from
sugar beet plants exposed to weed-reflected light in the greenhouse
study. Sugar beet did not increase petiole length in response to shade
avoidance cues as we had predicted based on previous work in other plant
species. This illustrates the importance of conducting research on crop
species with different growth habits, rather than generalizing from more
commonly studied species like Arabidopsis , maize, and soybean.
The reduction in sugar beet leaf size and leaf number reduced leaf
biomass, and subsequently, reduced root biomass (Figure 6). It is clear
from our results that weeds present at sugar beet emergence had a
significantly greater impact on sugar beet growth compared to weeds
added later in the season. Many previous studies have also shown that
early emerging weeds have a substantial effect on sugar beet yield.
Early weed removal is often recommended in sugar beets
(Jalali & Salehi, 2013). Our results
demonstrate that a substantial portion of reduced yield due to weeds may
be due to shade avoidance, rather than solely resource depletion as is
commonly thought. To protect sugar beet yield potential, ensuring a
weed-free environment at emergence may be critical.
It is important to state that crop yield loss due to shade avoidance is
typically understood in the context of consistent FR light stimulation,
but our understanding of shade avoidance responses at the molecular
level is not well-connected to whole-plant responses in agronomically
relevant contexts (Guo et al., 2017;
Shikata et al., 2014). Alternative
splicing occurs in response to far-red light at the seed stage, and
changes development into the seedling stage, but the effects on further
growth are not well understood after this point
(Penfield, Josse, & Halliday, 2010;
Shikata et al., 2014). There is evidence
that phytochrome interacting factor (PIF) proteins are upregulated
specifically in response to weed competition, although these do not
occur in all species (Horvath et al.,
2019; Horvath et al., 2015;
Page, Tollenaar, Lee, Lukens, & Swanton,
2009). The gene which controls leaf area index (LAI) during the shade
avoidance response is also involved in growth-phase transition and thus,
can affect organ size and whole-plant biomass
(Fu et al., 2012;
Toriba et al., 2019;
Wang, Schwab, Czech, Mica, & Weigel,
2008; Wu et al., 2009;
Xie et al., 2017). This latter
observation is particularly intriguing in light of differential leaf
area development shown in Figure 3, that a CoSAR can play a significant
role in crop yield loss opens a potential pathway for improved breeding
and bioengineering strategies.
We conclude that sugar beet exhibits a constitutive shade avoidance
response when exposed to early-emerging weeds causing season-long
impacts that affect growth, development, and yield potential. Thus, this
work has significant practical implications for weed management (e.g.
timing of weed removal) as well as crop genetic improvement. However,
our study system ensured a strong reflected R:FR light ratio at the time
of sugar beet emergence, and the weed density or proximity of weeds to
the sugar beet plants required to cause a similar response under more
typical field conditions remains unknown. This will no doubt vary by
weed species [e.g. differences in reflectance, growth habit (erect vs
prostrate), etc], crop row spacing, and other agronomic factors.
Although it is uncommon for weeds to be extremely dense in the field at
the time of sugar beet emergence, there is growing interest in ‘planting
green’, where a cash crop is seeded directly into established cover
crops, and this work suggests that practice may have unforeseen impacts
on crop yield potential.
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Table 1. Treatment descriptions showing the start and end of weed
treatments in growing degree days (GDD)