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.