Shading mediates the response of mycorrhizal maize (Zea mays L.) seedlings under varying levels of phosphorus
Introduction
Arbuscular mycorrhizal (AM) fungi belonging to phylum Glomeromycota (Wijayawardene et al., 2020) establish a mutualistic association with a majority of the terrestrial vascular plant species (Smith and Read, 2008). The carbon‑phosphorus (CP) relationship between the host plant and AM fungi is recognized as the most important functional trait for understanding the AM symbiosis. It has been found that C allocation by plants to AM fungi ranges from 4% to 20% (Smith and Read, 2008; Jakobsen and Rosendahl, 1990; Grimoldi et al., 2006; Calderón et al., 2012; Lendenmann et al., 2011). The plant photosynthate (e.g., plant C) is transferred to the fungus in the form of sucrose, hexose, or lipid across the mycorrhizal intraradical structures (e.g., hyphae or arbuscules in the root cortex) (Wipf et al., 2019; Jiang et al., 2017), and transported as glycogen, triacylglycerol and lipid through the extensive extraradical hyphae network (Bago et al., 2002, Bago et al., 2003; Jiang et al., 2017). The C allocation to AM fungi is affected by many factors such as light intensity (Zheng et al., 2015), soil P levels (Zheng et al., 2013), and AM fungal species (Smith et al., 2003; Zheng et al., 2015). Therefore, an in-depth understanding of the dynamics of mycorrhizal symbiotic C allocation under the changing P supply and light intensity is a matter of great interest.
Light intensity is a common factor affecting crop growth and yields under different field conditions (Konvalinková and Jansa, 2016). Light may significantly affect the photosynthetic rate and result in C accumulation in plants with different levels (Zheng et al., 2015), while P supply affects leaf photosynthesis and plant growth, ultimately affecting the CP interaction. The plant response to inoculation by mycorrhizal fungi was weak as the light decreased (Son and Smith, 1988; Hunt and Hope-Simpson, 1990). The previous studies also showed the reduced investments in AM fungi with the decline of the light intensity, resulting in reduced AM fungal colonization rate (Clark and Clair, 2011) and alter the physiology of AM fungi (Johnson et al., 2006). The plants under low light allocate more biomass to the aboveground plant structures while less biomass to AM fungi maintains the resource economics (Johnson, 2010; Johnson et al., 2014). For example, Konvalinková and Jansa (2016) showed that plants did not provide more C to AM fungi under the shading condition. By contrast, Friede et al. (2018) showed that shading did not exacerbate C costs to AM fungi. The other previous studies showed that the effect of shading on mycorrhizal response is P-dependent. For instance, shading significantly reduces the distribution of C to AM fungi under low P (7 mg kg−1) but not at high P (Zheng et al., 2015). A recent finding shows that plants transferred more C to the beneficial AM fungi, while the rewarding AM fungi may preferentially allocate P to the plant host (Ji and Bever, 2016). Hence, the CP relationship is very complex and may be plant-fungal-environment dependent. In accordance with the mutualism-parasitism continuum theory (Klironomos, 2003; Mariotte et al., 2013), the previous studies have shown that plant growth is inhibited when plants could not compensate the C demand of AM fungi (Hammer et al., 2011; Johnson, 2010; Johnson et al., 2014). Similar reports are well demonstrated for AM fungal mediated P uptake. For example, Zheng et al. (2013) showed that plants with P supply levels less than 50 mg kg−1 produced positive mycorrhizal P response (MPR), while the mycorrhizal response was negative at high P supply. AM fungi outcompeted with plants to maintain their growth, and thus P delivery to plants was reduced at extremely low P conditions (Antunes et al., 2012). P fertilization may shift the relationship between host plants and AM fungi from mutualism towards parasitism (Johnson et al., 1997; Verbruggen and Kiers, 2010) by suppressing AM fungal colonization (Al-Karaki and Clark, 1999; Wang et al., 2016). Specific genes encoding phosphate (Pi) transporters were upregulated in roots upon colonization by AM fungi (Smith and Smith, 2011). One such gene in maize is ZmPht1;6, an AM fungi inducible Pi transporter gene (Nagy et al., 2006), which takes up Pi from the cortical apoplast surrounding mycorrhizal structures (Glassop et al., 2005; Javot et al., 2010; Hata et al., 2010). P fertilizer supply suppressed the expressions of ZmPht1;6 in maize roots (Wang et al., 2016). Meanwhile, photosynthetic products are related to P deficiency-induced gene expressions. Previous results showed that signaling of P deficiency-induced gene expression requires sugar that phloem transported (Liu et al., 2005, Liu et al., 2010; Lin et al., 2014). Therefore, comprehensive research is needed to understand better how the shading mediates the interchange of carbohydrates and gene expression at different P levels.
This experiment was designed to explore the interactions of light and P on mycorrhizal maize seedlings response. Maize leaves were shaded by means of covering the leaves with aluminum folio, and three levels of P were supplied in the soil. R. irregularis and F. mosseae were selected as inocula. The specific Pi transporter gene in maize (ZmPht1;6 expression level) mediated by AM fungi (Nagy et al., 2006) was determined. We hypothesized that shading reduced the sensitivity of plant response to P supply, both in terms of plant growth and P uptake, and different AM fungal species showed the difference in mediating the CP interactions.
Section snippets
AM fungal inoculum
The AM fungal inoculum used in this study includes the Rhizophagus intraradices (R. intraradices, BEG141) and Funneliformis mosseae (F. mosseae, BEG 167), obtained from the Institute of Plant Nutrition and Resources, Beijing Academy of Agriculture and Forestry Research, Beijing. The fungal inoculum consisted of spores, mycelium, and the fine root segments and propagated in a 5:1 (v/v) mixture of zeolite and river sand with Zea mays L. grown for four months in a greenhouse.
Soil, plants, and experimental design
The soil was collected
Mycorrhizal colonization
Shading had no significant effect on root colonization rates of maize plants inoculated with F. mosseae or R. intraradices at all three P levels (Tables 1, S1). The root colonization rate of maize inoculated with R. intraradices was significantly higher than that of F. mosseae (Table 1). At three P levels, the root colonization rates of maize inoculated with F. mosseae were 60%, 78%, and 60% under the non-shading treatment, while 58%, 71%, and 62% for the shading treatment, respectively. The
The effects of shading on C transport with different AM fungal species and P supply level
Our results showed that shading significantly reduced the sugar concentration in phloem saps of mycorrhizal plants (Figs. 1, S1), indicating that light is a significant factor that substantially affects the transfer of carbohydrates from shoots to roots in mycorrhizal plants. Carbohydrates are synthesized by photosynthesis and transported to the various organs of plants in the form of sucrose or hexose (Wipf et al., 2019), through phloem for plant growth and development (Lu, 2003; Püschela
Conclusion
Our results showed that shading, P supply, and inoculation co-determine the distribution of photosynthate to plant and root system, where inoculation improved maize adaptability under shading stress conditions. Shading significantly reduced the soluble sugar concentration in the phloem of mycorrhizal maize seedlings, but had no significant effect for non-mycorrhizal treatment. The root biomass and root-shoot ratio of mycorrhizal maize decreased significantly under shading treatments regardless
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was supported by the National Key Research and Development Program of China (2017YFD0200200 and 2017YFD0200202), National Natural Science Foundation of China (Grant No. 32002126), Fundamental Research Funds for the Central Universities (XDJK2019C065) and the National Natural Science Foundation of China (Grant No. 41601244).
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