Abstract
As an essential regulator of photosynthesis and hormone signaling, light
plays a critical role in leaf senescence and yield gain in crops.
Previously, numerous studies have shown that the narrow-wide-row
planting pattern, especially under intercropping systems, is more
beneficial for crops to enhance light interception, energy conversion,
and yield improvement. However, the narrow-wide-row planting pattern
inevitably leads to a heterogeneous light environment for crops (i. e.,
maize in maize-based intercropping systems) on both sides of the plant.
The mechanism by which it affects leaf senescence and yield of maize
under a narrow-wide-row planting pattern is still unclear. Therefore, in
this study, we compared the leaf senescence and yield formation process
of maize under homogeneous (normal light, NL and full shade, FS) and
heterogeneous (partial light, PL) light conditions. Results revealed
that partial light treatment influenced the homeostasis of growth and
senescence hormones by regulating the expression of ZmPHYA and ZmPIF5.
Compared to normal light and full shade treatments, partial light
delayed leaf senescence by 3.6 and 5.9 days with 2.2 and 3.3 more green
leaves and 1.1 and 1.4 fold nitrogen uptake, respectively. Partial light
reduced oxidative stress by enhancing antioxidant enzyme activities of
PS (shade side of partial light) leaves, which improved photosynthetic
assimilation, balanced sucrose, and starch ultimately maintaining the
similar maize yield to NL. Overall, these results are important for
understanding the mechanism of leaf senescence in maize, especially
under heterogeneous light environments, which maize experienced in
maize-based intercropping systems. Furthermore, these findings are
providing proof of getting a high yield of maize with less land in
intercropping systems. Thus, we can conclude that maize-based
intercropping systems can be used for obtaining high maize yields
maintained under the current climate change scenario.
Key-words : maize; heterogeneous light; leaf senescence;
phytohormone; phytochrome
Introduction
Leaf senescence (LS) is an age-dependent, genetically regulated process
(Sakuraba et al., 2014) and is considered
the last stage of leaf development
(Brouwer et al., 2012). Therefore, as a
declining phase of leaf development, it induces several catabolic
activities in leaves. For instance, LS includes the degradation of
protein, nucleic acids, and chlorophyll, destabilization of
intercellular organelles, and limiting the remobilization of nutrients
to developing tissues and storage organs
(Buchanan-Wollaston et al., 2003;
Leopold, 1961;
Masclaux-Daubresse et al., 2008;
Smart, 1994). Besides aging, various
environmental stresses, like low light conditions, drought, salinity,
and high or low temperature, can also initiate the process of LS during
plant growth and development (Lim et al.,
2007). Interestingly, moderate stress stimulation, depending on the
interaction of environmental factors and phytohormone signals, could
create an adaptive balance between plant growth and defense
(Brouwer et al., 2012;
Matyssek et al., 2002). In the above
studies, all plants grow in a homogeneous environment. However, the
molecular communication to regulate the carbon metabolism and signaling
of plant hormones between the two sides of a plant to regulate leaf
senescence and overall yield under a heterogenous light environment
still invites a deep investigation at the physio-molecular level.
Earlier, genetic investigations in Arabidopsis thaliana have
discovered numerous senescence-associated genes (SAGs) and the genes
associated with plant hormone signaling
(Lim et al., 2007). Generally, auxin
plays an important role in suppressing leaf senescence
(Lim et al., 2003). Decreased auxin
levels may signal or enhance the onset of senescence, and levels of IAA
reduce as a result of LS in various plants
(Jiang et al., 2014;
Kim et al., 2011;
Shoji et al., 1951;
Uzelac et al., 2016). Several Auxin
Response Factors (ARF) affect different aspects of senescence depending
upon the target promoters (Tiwari et al.,
2003). Previously, ARF2, ARF7, and ARF19 have been reported as
repressors for auxin signals and suppress the expression of
senescence-associated genes (SAGs) (Ellis
et al., 2005; Lim et al., 2010;
Lin & Wu, 2004). Another important
phytohormone, gibberellin, promotes senescence on the transition from
vegetative to reproductive growth. Therefore, plants exhibited
precocious developmental senescence upon applying bioactive GA3 and the
absence of GA pathway repressor DELLAs
(Schippers et al., 2015). Notably, the
mode of action and the influence of different phytohormones over the
regulation of senescence mechanism vary among different plant hormones.
Like, ethylene signaling or biosynthesis genes directly regulate the
time of senescence while the increased abscisic acid level in leaves
promotes chloroplast degradation and repress chloroplast biosynthesis
genes (Bennett et al., 2014;
Liang et al., 2014). Furthermore, the
treatment of plants with jasmonic or salicylic acid accelerated the
senescence (Ueda et al., 1981; Morris et al., 2000), in contrast,
application of cytokinins delayed the senescence (Gan and Amasino,
1995). Similarly, the knockout of ethylene receptor1-1 andabscisic acid receptor 9 enhance stress resistance and delay leaf
senescence (Grbic & Bleecker, 2010;
Zhao et al., 2016). Taken together, it
establishes the fact that the study of the individual role and mutual
interaction of various plant hormones are very important to investigate
the signaling and development of plant growth stages under prevailing
environmental conditions. However, the mechanism involving the change in
phytohormone levels and their interaction to regulate leaf senescence
under a heterogeneous light environment, particularly under the
circumstances of intercropping systems, is still unclear.
Different light environments could impact photosynthetic carbon fixation
and its regulation by directing the leaf senescence, which could
influence plant growth and development at a later stage
(Grbic & Bleecker, 2010;
Velerskov, 2006). For instance, in a
wide-narrow planting pattern, the crop is exposed to different light
conditions, i.e., wide row (light side) and narrow row (shade side). In
this perspective, some latest studies showed that narrow-wide row
planting patterns changed the light environment and affected the carbon
balance and senescence (Chen et al.,
2020; Feng et al., 2020). Interestingly,
half shading improved the photosynthesis and light utilization
efficiency of maize leaves (Huang et al.,
2019; Sun et al., 2019). Earlier, it was
also shown that low light conditions induce or delay the leaf senescence
process depending on the photosynthetic health of the plants
(Keech et al., 2007;
Keech et al., 2010). Similarly, the LS
process of older leaves was reduced when plants were allowed to grow
under darkness or shaded conditions
(Tadahiko et al., 1993;
Trejo-Arellano et al., 2020). Moreover,
the delay in LS was reported to influence the productivity of
intercropped species by prolonged grain filling time, increased resource
use efficiency, and high land equivalent ratio
(Chen et al., 2020;
Feng et al., 2020). Therefore, the
light-influenced senescence of leaves could affect the seed yield and
seed quality of crops (Buchanan-Wollaston
et al., 2003; Lam, 2004). Altogether,
these reports suggest a deep understanding of the LS process under
different growth conditions as an essential prerequisite for optimizing
the light use efficiency and yield of multiple-cropping systems.
The maize soybean intercropping system hosts a diverse light environment
in quantity and quality. Consequently, varying abundance of red light
and far-red light (FR) could influence the response of different light
receptors and phytohormones which could induce different senescence
processes of leaves in intercropped maize. For instance, under partial
shade, FR light receptor phytochrome A (PHYA), which maintains the leaf
chlorophyll content, does not induce leaf senescence directly, while red
light receptor phytochrome B (PHYB) mediates leaf senescence in the
whole shading process (Brouwer et al.,
2014; Lim et al., 2018). It has been
reported that the Pfr form of phyB inhibits LS by repressing PIF4/PIF5
at the transcriptional and post-translational levels, respectively.
Notably, in the dark, these PIF4/PIF5 directly activate the two bZIPs
(ABI5 and EEL) and EIN3 (Sakuraba et al.,
2014). Interestingly, shade-induced senescence of leaves can be
prevented by limiting the shade duration with red light. Upon
transferring to normal light conditions, FR light can also initiate LS
(Pons & de Jong, 2004;
Rousseaux et al., 1997). Due to this, the
low-light-induced LS at higher planting densities has been ascribed to
the relative increase in FR light (Barreiro
et al., 1992; Rousseaux et al., 1996).
On the other hand, numerous scientists have reported that initiation of
the LS depends on light quantity compared to light quality
(Brouwer et al., 2012;
Sakuraba et al., 2014). Similarly,
several reports have proposed that when the quantity of light decreases
below the photosynthetic-light-compensation-point (LCP), it decreases
the carbon production in plants by reducing the photosynthetic rate
enhanced LS (Boonman et al., 2006). Such
reports indicate that improved light conditions in agricultural fields
can reduce the LS of crops at higher planting densities or under
intercropping systems. Therefore, to ascertain the role of light in
intercropping, a deep investigation about the response of maize plants
under differing light environments is required.
Notably, the maize soybean intercropping systems can guarantee maize
yields with less land comparable to sole cropping and obtain an
additional soybean yield. How is it possible? This research aimed to
explore why maize leaf senescence was delayed and how the heterogenous
light-induced phytohormone changes and carbon communication under this
system. Given the dichotomous light conditions around maize plants in
intercropping systems, we hypothesized that the two side leaves could
express different regulatory mechanisms that could influence the overall
growth and metabolism in maize plants. Therefore, we adopted a simulated
approach to verify our hypothesis and designed an in-depth investigation
about the metabolic and leaf senescence regulations at the
morphological, physiological, and molecular levels.