Partial shading improves photosynthetic performance by
increasing leaf greenness and delaying LS
It has previously been reported that plants exhibit different metabolic
strategies in different light intensities
(Keech et al., 2007). Maize leaves are
highly sensitive to slight changes in light intensity, and any decrease
in light intensity affects photosynthetic performance
(Feng et al., 2019), which results in a
change in leaf greenness, as shown in the current study. We attribute
the delayed senescence in maize leaves as a contributor to increased
plant photosynthetic capacity and carbon balance. The results indicate
that partial shading delays the leaf senescence process in maize
compared to NL, possibly via an enhanced photosynthetic process.
However, the light interception by the whole plant is also important in
the delayed leaf senescence process. For instance, our results of
different partial shading degrees showed that 20% shading would delay
leaf senescence, maintain leaf greenness and nitrogen content, prolong
the senescence time of bottom leaves, and increase the leaf area
(Supporting Information Figure S5, Table S2).
Improved photosynthetic performance is required for balanced growth in
plants. In the present study, partial shade remarkably increased maize
photosynthetic ability compared to full shade. Evidence has demonstrated
that shade changes a plant’s micro-climate, which disrupts a plant’s
photosynthetic performance, growth activity, and reduced yield
(Gindaba & Midgley, 2005), while the
right amount of shading improves plant growth and photosynthetic
performance (Han et al., 2018).
Consistent with the present study data, NL significantly reduced
photosynthetic performance in maize plants, while partial shading
improved the photosynthetic performance in maize plants. We observed
that all the photosynthetic characteristics, Chl b, and nitrogen content
were increased under partial shade (Fig.1, Supporting Information Figure
S3). According to the results (Hachiya &
Noguchi, 2011), the high transcription of nitrogen transporter geneZmNRT1.1a may maintain the nitrogen content and chlorophyll
protein stability in PS leaves. Furthermore, the expression of
chlorophyll degradation-related genes (ZmPaO ) increased at first
ten days then stayed unchanged in PS, however in NL treatment, the
expression level constantly increased during the whole experimental
period, indicating leaves chlorophyll degradation in PS was reversed but
continued to rise in NL (Fig. 7). Chlorophyll content and degradation
process were positively correlated with aging senescence. We speculate
that a possible mechanism is used by partial shade to enhance delay in
leaf senescence in maize. We hypothesized that the improvement in the
photosynthetic performance during the partial shade treatment might
result from enhancement in plant hormonal balance under the partial
treatment (Clarke et al., 2009;
Wang et al., 2010). Others also reported
that delay in leaf senescence could improve plant photosynthetic
performance, which could, in turn, increase plant yield
(Gregersen, 2011), which is consistent
with our results (Table 3). Together, these results suggest that partial
shade delays leaf senescence in maize by enhancing the photosynthetic
rate and inhibiting chlorophyll degradation.
How Partial Shade Coordinates Phytohormones homeostasis
to Regulate Leaf Senescence?
Phytohormones and their related genes regulate plant growth and
development under various stresses (Bawa et
al., 2020a; Bawa et al., 2020b;
Tang et al., 2019). Indeed, all major
plant hormones have been reported to play an important role in leaf
senescence regulation (Schippers et al.,
2007) by altering the time of age-related changes and interacting with
the prevailing environmental conditions, thus influencing the speed of
the overall senescence process (Jibran et
al., 2013). Similarly, in the present study, we hypothesized that
different light regimes might influence the hormonal regulations between
the two sides of the maize plant, impacting leaf senescence. For
instance, phytohormones like ethylene, abscisic acid (ABA), and
salicylic acid (SA) accelerate the senescence process in contrast
accumulation of auxin, gibberellin, and cytokinin delay senescence
(Guo & GAN, 2012;
Jibran et al., 2013). Previously,
increased accumulation of some plant hormones such as IAA and
GA3 under slight shading has been reported as growth
promotion indicators (Han et al., 2018).
Consistent with these findings, our results showed that the partial
light conditions induced significant accumulation of IAA, ABA,
GA3, and ethylene, specifically in PS leaves. The IAA
content in PF leaves also increased; suggesting that some key factors
might regulate phytohormone balance and limit leaf senescence in PS
treatment (Fig. 9). PIF4 binds promoters of TAA1 , CYP79B2 ,
and YUCCA8 genes to promote auxin biosynthesis at high
temperatures (Sun et al., 2012;
Wang et al., 2017a). In the current
study, may be a similar mechanism of ZmPIF4 controls the IAA
level in maize leaves under PS treatment. PIF4 and PIF5 regulated GA
biosynthesis via a circadian clock factor ELF3 as loss of ELF3 activity
caused GA accumulation. Moreover, PIF4 is also involved in activating
transcription factors EIN3 and ABI5 to regulate leaf senescence. In the
present study, PIF5 and not PIF4 might play a key role in maintaining
phytohormone balance because only PIF5 was strongly induced by the PS
treatment (Fig. 6B). Another protein expression data of full shade
leaves showed that continuous shading could significantly influence the
expression of PHYA and EIN3 that leads to leaf senescence (Supporting
Information Figure S6). However, the senescence inducing hormones (ABA
and ethylene) decreased significantly during the succeeding days which
could be a reason for the delayed leaf senescence under the partial
light conditions.
Photoreceptors recognize the light conditions in plants, and as a
component of light signaling, they are associated with leaf senescence
(Kim et al., 2017). In this perspective,
identifying some major transcription factors (TFs) that play a crucial
role in leaf senescence through TFs-mediated senescence regulations has
enhanced the importance of TFs-mediated senescence regulation.
Therefore, we investigated the expression of several transcription
factors that are involved in light signaling and phytohormone responses
like ZmPHYA1b (Zea maize Phytchrome A1 b),ZmPIF4.1 (Zea maize Phytochrome Interacting factor 4.1),ZmPIF5.1 , ZmEIN3.1 (Ethylene Insensitive 3),ZmABI5.1 (ABA Insensitive 5) and SAG (Senescence associated
genes) to verify their contribution in the regulation of leaf senescence
under the different light regimes in maize plants. Several reports have
suggested the involvement of PIFs in dark-induced and developmental
senescence as they transduce light information to primary senescence
regulators (Kim et al., 2017). PIF4/PIF5
acts in the signaling pathways of two senescence-promoting hormones,
ethylene and abscisic acid, by directly
activating the expression of EIN3,
ABI5, and EEL (Sakuraba et al., 2014).
Similarly, in our study, during the first ten days under partial light
conditions, the PS leaves of maize plants showed significant
upregulation of ZmPHYA1b , ZmPIF4.1 , and ZmPIF5.1,
ZmABI5.1, and ZmEIN3.1 genes (Fig. 6A). Here, PIF4 protein was
not expressed in NL and PL treatments. However, in FS, the expression of
PIF4 was significantly induced by early full shading. The same results
were found in PHYA, PIF5, EIN3, indicated heavy shade would certainly
lead to rapid leaf senescence (Fig. 6B). Contrarily, their expression
was suppressed in the PF leaves compared to NF, NS, and PS. It shows
that the leaves under PF conditions compensated the leaves on the other
side of the maize plant to counter the influence of shading which could
be a reason for delayed leaf senescence. In agreement with our results,
different studies reported the activation of senescence-related genes inA. thaliana under partial shading
(Brouwer et al., 2014). However, our
research found that heterogenous shading under PL conditions induced a
regulatory mechanism between the two side leaves. The PF leaves balanced
the initial increase of senescence regulators in PS leaves.
Several senescence-associated genes (SAGs) have been identified in
Arabidopsis, wheat, rice, and maize that have been linked to the
complicated and highly regulated process of leaf senescence
(Li et al., 2014;
Wu et al., 2016). Therefore, to further
verify the information revealed through phytohormone signaling
regulation and expression of relevant transcription factors, we
quantified maize SAGs. Notably, the reduced expression of ZmSAG2and ZmSAG12 in PS and significant reduction after an initial
increase in the first ten days under partial light conditions suggested
a synergy between the two side leaves. This observation verified the
delayed leaf senescence under partial light conditions in maize (Fig.7).
Furthermore, in agreement with our hypothesis, seed dry matter
accumulation increased from day 5 up to day 25 under NL. In contrast,
partial shading increased dry seed matter accumulation from day 5 up to
day 35 (Fig. 8), which could be due to increased leaf greenness under
partial light conditions. Collectively, it could be displayed from the
hormonal signaling and expression pattern of senescence-related TFs that
the decrease in light intensity improved the growth response and
greenness of maize leaves due to the compensatory interaction between
the two lateral sides of the maize plant under heterogeneous light
conditions.