Maize/peanut intercropping increases photosynthetic characteristics,13C-photosynthate distribution, and grain yield of summer maize

Ll Yan-hong , SHl De-yang , Ll Guang-hao ZHAO Bin ZHANG Ji-wang LlU Peng REN Baizhao DONG Shu-ting

1 State Key Laboratory of Crop Biology/College of Agronomy, Shandong Agricultural University, Tai’an 271018, P.R.China

2 Soil Fertilizer Station of Yantai Agricultural Technology Promotion Center, Yantai 264000, P.R.China

3 Institute of Maize and Oil Crops, Yantai Academy of Agricultural Sciences, Yantai 265500, P.R.China

Abstract Intercropping is used widely by smallholder farmers in developing countries to increase land productivity and profitability. We conducted a maize/peanut intercropping experiment in the 2015 and 2016 growing seasons in Shandong, China. Treatments included sole maize (SM), sole peanut (SP), and an intercrop consisting of four rows of maize and six rows of peanut (IM and IP). The results showed that the intercropping system had yield advantages based on the land equivalent ratio (LER)values of 1.15 and 1.16 in the two years, respectively. Averaged over the two years, the yield of maize in the intercropping was increased by 61.05% compared to that in SM, while the pod yield of peanut was decreased by 31.80% compared to SP.Maize was the superior competitor when intercropped with peanut, and its productivity dominated the yield of the intercropping system in our study. The increased yield was due to a higher kernel number per ear (KNE). Intercropping increased the light transmission ratio (LTR) of the ear layer in the maize canopy, the active photosynthetic duration (APD), and the harvest index (HI) compared to SM. In addition, intercropping promoted the ratio of dry matter accumulation after silking and the distribution of 13C-photosynthates to grain compared to SM. In conclusion, maize/peanut intercropping demonstrated the potential to improve the light condition of maize, achieving enhanced photosynthetic characteristics that improved female spike differentiation, reduced barrenness, and increased KNE. Moreover, dry matter accumulation and 13C-photosynthates distribution to grain of intercropped maize were improved, and a higher grain yield was ultimately obtained.

Keywords: maize, intercropping, peanut, land equivalent ratio (LER), net photosynthetic rate (Pn), 13C-photosynthates distribution

1. lntroduction

Intercropping, usually defined as the growing of two (or more) crops simultaneously on the same area of ground(Willey 1990), has potential advantages such as higher overall productivity, better pest and disease control, and enhanced ecological services (Snapp et al. 2010; Finch and Collier 2012). Historically, in China, intercropping has played a very important role in ensuring crop production and increasing the income of farmers (Tong 1994; Yang 2011).China has more than 22% of the world’s population but less than 9% of the world’s arable land, and the competition for land for cropping grain and oil crops has become more serious. Maize (Zea mays L.) is one of the major food and feed crops, and peanut (Arachis hypogaea L.) is an important oil crop in China, where its total output reached 1.729×1010kg in 2016, ranking the first among oil crops (Liu et al. 2017). Maize/peanut intercropping can significantly alleviate the competition for land between maize and oil crops and achieve synchronous increases in the yields of grain crops and oil crops (Zuo et al. 2000).

Maize is a common crop in most intercropping systems,and an abundance of research has shown that the yield of maize intercropped with pea bean (Phaseolus vulgaris L.),broad bean (Vicia faba L.), soybean (Glycine max L.), or peanut is significantly higher than that of monoculture maize.The greater maize yield in intercropping systems improved land productivity, resulting in obvious yield advantages for intercropping (Tsubo et al. 2005; Li et al. 2007; Hugar and Palled 2008; Banik and Sharma 2009; Postma and Lynch 2012). Other investigators have shown that intercropping of Poaceae and Fabaceae produces higher seed yields than either pure crop (Mpairwe et al. 2002; Mucherumuna et al.2010). However, Wang et al. (2016) suggested that maize/alfalfa intercropping yields were reduced compared to those in monoculture, but that the economic benefit was increased compared to that in monoculture. Coll et al. (2012) reported that intercropping sunflower and maize resulted in a 20%lower grain yield than for sole crops, demonstrating that not all combinations of crops in an intercropping system result in mutual benefits.

Previous studies have pointed out that maize/peanut intercropping would help increase production through efficient utilization of resources such as solar energy,water, and nutrients (Zhang and Li 2003; Awal et al. 2006;Xu et al. 2008; Zhang et al. 2012). The intercropping system is a three-dimensional optical system that has large light-specific surface area (Black and Ong 2000)that can increase the interception of side light. Moreover,this multi-level crop group can maximize the use of solar radiation and realize crop utilization of stratified light energy,as well as stereoscopic and efficient use (Cui et al. 2015),thereby increasing dry matter accumulation. The relative contributions to increased biomass have been shown to be two-thirds from the border rows effect and one-third from the inner rows effect (Li et al. 2001). Little is known about the branch row from quantitative studies on maize, although intercropping systems are widely applied; therefore, we conducted a two-year field experiment. The objectives of the work were (i) to investigate the influence of the margin effect on photosynthetic productivity of intercropped maize compared with monoculture maize and (ii) to evaluate the accumulation and distribution of13C-photosynthate and dry matter of maize with the13CO2stable isotope tracer to obtain an improved understanding of the effect of intercropping on maize yield. This study will provide valuable information for the adjustment of agricultural structure and sustainable development of agriculture.

2. Materials and methods

2.1. Experimental site

A field experiment was conducted in 2015 and 2016 at the Corn Technology Innovation Center of Shandong Agricultural University (36°10′N, 117°09′E), Tai′an, Shandong Province,China. The soil type was a sandy loam consisting of 11.27 g kg-1organic matter, 0.92 g kg-1available N, 47.18 mg kg-1available phosphate, and 84.2 mg kg-1available potassium in the top 0-20 cm arable soil layer. Precipitation(mm) and air temperature (°C) were measured by an automatic weather station (Fig. 1).

2.2. Experimental materials and design

The experiment included three planting patterns with maize(cv. Denghai 618) and peanut (cv. Huayu 22): sole maize(SM) cropping, sole peanut (SP) cropping, and intercropping system (intercropped maize, IM; intercropped peanut,IP). SM was planted at a density of 105 000 plants ha-1,an inter-row distance of 60 cm, and an intra-row distance of 15.9 cm. SP was planted with a density of 180 000 holes ha-1(two peanuts per hole), an inter-row distance of 35 cm, and an intra-row distance of 16 cm. The intercropping system was planted in 4:6 pattern, that is, four rows of maize and six rows of peanut. With this row-ratio design,the two crops cover a similar area, which facilitates rotation of the two crops to eliminate continuous peanut obstacles.Maize and peanut were planted at the same density in their strips in the intercropping system as in their respective monocultures. The distance between the maize and peanut strips was 50 cm (Fig. 2). The plot size was 6 m in width by 20 m in length in SM, 7 m in width by 20 m in length in SP, and 13.65 m in width by 20 m in length in the maize/peanut intercropping system. The row orientation was northsouth with three-time repetition. Furthermore, to eliminate differences among duplications, six rows of peanut and then several rows of maize were planted at the left of the maize/peanut intercropping system, and four rows of maize and then several rows of peanut were planted at the right of the intercropping system. Basal fertilization of each subplot,with fertilizer applied before tillage on 5 June during both years, included nitrogen as resin-coated urea, phosphorus as calcium superphosphate, and potassium as potassium chloride at rates of 200 kg ha-1N, 100 kg ha-1P2O5, and 120 kg ha-1K2O, respectively. Maize and peanut seeds were planted with hand planters on 10 June 2015 and 2016. The harvest dates were 5 October 2015 and 2016. It should be noted that the two crops were rotated in the 2016 growing season. In addition, irrigation, weeds, diseases,and insect pests were controlled adequately during each growing season so that no factor other than planting pattern limited growth.

Fig. 1 Maximum, minimum, and mean temperatures and precipitation recorded during the growing seasons in 2015 and 2016.

Fig. 2 Schematic illustration of row placement of maize and peanut in intercropping system. L1-L4 denote the number of rows of maize from west to east.

2.3. Sampling and measurements

Land equivalent ratio (LER)The yield effectiveness of an intercrop is valued using the concept of the LER, which is used to obtain evidence about whether two or more crops should be intercropped rather than planted as sole crops(Rao and Willey 1980):

where Yaand Ybare the yields of each crop in the intercrop,Maand Mbare the yields for each monoculture, and LERaand LERbare the partial LERs for each species. An LER of 1.0 indicates the same land productivity for intercropping and for sole cropping, values greater than 1.0 indicate a land use advantage for intercropping, and values smaller than 1.0 indicate a disadvantage for intercropping.

Yield, yield components, dry matter weight (DM),and harvest index (Hl)The yield and DM of maize and peanut were measured when plants were mature. For maize, 5-m-long row sections, which were not destroyed by sampling, were sampled in each plot. Three center rows in sole-cropped plots and four rows (from L1 to L4) in intercropped plots were selected for harvest. These were used to investigate yield and yield components. The kernel number per ear (KNE) was counted for all of the harvested ears. Three samples of 1 000 kernels were oven-dried at 80°C for three days to constant weight and weighed to estimate thousand-kernel weight (TKW). All of the kernels were air-dried to investigate yield, and grain yield was expressed at 14% moisture. In addition, five plant samples were obtained from the center of the sole-cropped plot and each row of the intercropped plot and subsequently dissected into ear leaf, other leaves, stem (including sheath),cob, tassel, ear bracts, and grain. All separated components were oven-dried at 80°C to constant weight and weighed to estimate DM (kg ha-1). HI was calculated by dividing the grain weight (adjusted to a moisture content of 0.14 g H2O g-1fresh weight) by the aboveground DM at physiological maturity. For peanut, 2-m-long row sections were sampled in each plot. Three rows were selected in the sole-cropped plot, and a full peanut strip was selected in intercropped plots. These were used to investigate yield. In addition,the yields for IM and IP were determined on an equivalent basis of comparable land area of the sole crops.

lntercropping incomeTo illustrate the economic rationale for intercropping, we used the following formula to calculate the gross income of the intercropping system:

Income of intercropping system=YIM×Fm×Pm+YIP×Fp×Ppwhere YIMand YIPrefer to the yield of intercropped maize and intercropped peanut, Fmand Fpindicate the proportion of maize area and peanut area in the intercropping system, and Pmand Ppare the price of maize and peanut, respectively.A current typical price for maize is 2 CNY kg-1, and peanut fetches approximately 5 CNY kg-1. In this study, Fmwas 0.505 and Fpwas 0.495.

Net photosynthetic rate (Pn) Pnwas measured in 2015 and 2016 with a portable gas exchange system (CIRAS-2, PP Systems, UK) equipped with a square (2.5 cm2) chamber.The photosynthetic photon flux density (PPFD), provided by an internal light source from the leaf chamber, was 1 600 μmol m-2s-1, and the leaf temperature was a relatively constant 30°C. The measurements were done at the tasselling stage(VT), kernel blister stage (R2), kernel milk stage (R3), and kernel dent stage (R5) from 10:00-12:00 a.m. on cloudless days in each row of IM and the center rows of SM.

Canopy light transmission ratio (LTR)The photosynthetic effective radiation of the ear layer was observed with a plant canopy digital image analyzer (CI-100, CID Bio-Science,Inc., USA) to calculate the light transmission ratio at VT, R2,R3, and R5. The LTR (%) is equal to the photosynthetic effective radiation of the determined layer divided by the photosynthetic effective radiation of the canopy layer multiplied by 100.

Distribution of 13C-photosynthates among plant organsWe performed a leaf labeling experiment with13CO2in the 2016 growing season. Ten representative plants in each row of maize in the intercropping system and the middle row in the sole maize were selected at the silking stage. We encased the ear leaf of each selected plant in a 0.1-mm-thick Mylar plastic bag, which permitted sunlight to pass at levels up to 95% of natural intensity. The bags were sealed at the base with plasticine and subsequently injected with 60 mL of13CO2. After allowing photosynthesis to proceed for 60 min, the13CO2in each bag was extracted through a KOH washer to absorb the remaining13CO2and the plastic bag was removed. This experiment was conducted from 09:00-11:00 a.m. on clear days.

Samples were collected at ground level from five labeled plants in the middle rows of SM and the border rows (L1 and L4) and the inner rows (L2 and L3) of the maize in the intercropping system at 24 h after labeling (24 h) and physiological maturity (R6). The plants were subsequently dissected into ear leaf, other leaves, stem (including sheath),cob, tassel, ear bracts, and grain. All of the separated components were over-dried at 80°C to constant weight,weighed to record dry matter (g/plant), and then ground into powder and passed through a 200-mesh sieve. Subsamples(4 mg each) were used to determine the isotopic abundance with an IsoPrime 100 instrument (Elementar, Cheadle, UK).The distribution of13C-photosynthates among different plant organs (%/plant) was then calculated.

2.4. Statistical analysis

Means and standard errors were calculated for individual measurements taken at each sampling date. Treatments were compared by analysis of variance using SPSS 17.0 Software (SPSS Institute, Inc.). To identify significant treatment effects, multiple comparisons were performed with the least significant difference (LSD) test, and the significance level was set at the 0.05 probability level.

3. Results

3.1. Yield and LER

The maize yields in 2015 and 2016 differed significantly between intercropped and sole-cropped treatments(P＜0.001) and between years (P=0.073) (Table 1). Grain yields of maize were greatly improved by the application of intercropping. Averaged over the years, the maize yield in the intercropped system was 16.68 t ha-1, which was 161.0%of the SM yield (10.36 t ha-1). However, intercropping significantly (P＜0.01) reduced the pod yield of peanut over the two growing seasons. Averaged over the two seasons,the peanut yield was 2.97 t ha-1, which was 68% of the SP yield (4.36 t ha-1).

LERs have been used historically to compare yields of intercropping systems with yields of sole-cropped species.In the 2015 and 2016 seasons, the LERs of the intercropped system were 1.15 and 1.16, respectively. Averaged over the two seasons, the LERs of maize and peanut were 0.815 and 0.34, which indicated that the advantage of intercropping was due mainly to the increase in maize yield.

3.2. Yield components for maize and border effects

With the same intra-row distance in SM and IM, the KNE of any row of IM was significantly higher than that of SM,similar to the result for ear number per 5-m row in the two years (Fig. 3). The contributions of border and inner rows to yield were also different in the intercropping systems. The KNE was significantly greater in border rows than in inner rows, whereas no significant difference in ear number per 5-m row was found between border and inner rows and no differences in TKW were found between IM and SM in both seasons (Fig. 3). In intercrops, border-row effects were positive for maize yield components (KNE, ear number per 5-m row, and TKW).

3.3. Canopy transmittance

For the two years, the LTR of the ear layer in IM was higher than that in SM at the corresponding growth stage (Fig. 4).The LTR of the ear layer in maize increased with the development of the growing stage; however, no significant difference was found between VT and R2 in each treatment.Averaged over the two years, the LTR values of IM at VT, R2,R3, and R5 were 102.7, 102.7, 104.1, and 66.3% higher than those of sole maize, respectively, which provided sufficient light for photosynthesis of leaves.

3.4. Pn

Intercropping increased the Pnof maize significantly in different growing stages in both seasons (Fig. 5). With the development of the growing stage, the Pnof ear leaves of SM and any row of IM showed a single-peak trend, reaching its maximum at R2, and then decreasing. Averaged over the two years, the Pnof L1 to L4 in IM at R2 increased by 20.3, 14.9, 14.4, and 19.2%, respectively, compared with SM, whereas it increased by 41.4, 33.1, 33.4, and 33.9%,respectively, at R5, which indicated that intercropping delayed the senescence process of maize, increased the active photosynthetic duration (APD) of functional leaves,and then increased the accumulation of photosynthetic products. Moreover, under the intercropping condition, the Pnof ear leaves in border rows was greater than that in inner rows, but no significant differences were found between border and inner rows.

3.5. Dry matter transportation and Hl

The effects of planting pattern and year were significant for total plant dry matter at R6, biomass accumulation after silking, and the ratio of dry matter accumulation after silking,whereas a significant effect of their interaction was observed only between total plant dry matter at R6 and biomass accumulation amount after silking (Table 2). Averaged over the two years, intercropping increased the total dry matterat R6 by 45.24% (border row) and 38.97% (inner row) vs.SM, and the biomass accumulation amount after silking was increased by 57.28% (border row) and 45.61% (inner row). In addition, intercropping significantly increased the HI of maize (P＜0.001), whereas no significant difference was found between border and inner rows of IM.

Table 1 Effects of cropping system on yield and land equivalent ratio1)

Fig. 3 Maize ear numbers per 5-m row (A and B), kernel number per ear (KNE, C and D), and thousand-kernel weight (TKW, E and F); L1-L4 denote the number of rows from west to east. IM, the maize in intercropped plot; SM, the maize in sole-cropped plot. Data for sole maize are indicated in row L1. Bars mean SE.

Fig. 4 Effects of planting pattern on light transmission ratio of maize in different growing stages from 2015 to 2016. SM, the maize in sole-cropped plot; IM, the maize in intercropped plot. VT, R2, R3, and R5 represent the tasseling, kernel blister, kernel milking,and kernel dent stages, respectively. Bars mean SE.

3.6. Dry matter allocation among different plant organs

The planting pattern significantly affected the partitioning of dry matter of maize to different plant organs at R6 (Table 3).There were significant effects of planting pattern (P＜0.001)and year (P=0.008) on the amount of dry matter in stem tissues, and there was also a significant interaction of plant pattern×year (P=0.064). On average, stem dry matter increased by 22.2 and 19.3% in border and inner rows of IM, respectively. The dry matter allocation in leaves was significantly influenced by planting pattern (P＜0.001) and the interaction of year and planting pattern (P=0.015), whereas the effect of year alone was not significant. In addition,there were significant effects of planting pattern (P=0.002)and year (P＜0.001) on the amount of dry matter in grain,whereas no significant effect was found for the interaction of planting pattern×year (P=0.390). On average, grain dry matter increased by 44.73 and 37.12% in border and inner rows of IM compared to SM.

3.7. Distribution of 13C-photosynthates in different organs at 24 h and R6

The planting pattern altered the pattern of distribution of13C-photosynthates among different organs (Table 4). At 24 h, the maximum ratio of distribution was recorded in stem, followed by leaves and ear bracts. Intercropping significantly reduced the rate of distribution into stem and ear leaf and increased the rate of distribution into ear bract,but no significant differences in these variables were found between border and inner rows in IM. At R6, intercropping significantly reduced the distribution of13C-photosynthates into stem, leaf, ear bract, and tassel, while it increased the allocation into cob and grain. The distribution of13C-photosynthates into grain was the largest for border rows of IM and the lowest for SM. Relative to SM, the13C-photosynthates distribution into grain increased by 7.5% in border rows of IM and 6.4% in inner rows of IM.In addition, significant differences in all organs, except for ear bracts, were found between border rows and inner rows of IM.

Fig. 5 Effects of planting pattern on net photosynthetic rate (Pn) of maize at different growing stages from 2015 to 2016. SM, the middle rows of maize in sole-cropped plot; IML1-IML4, the number of rows from west to east in intercropped plot. VT, R2, R3, and R5 represent the tasseling, kernel blister, kernel milking, and kernel dent stages, respectively. Bars mean SE.

Table 2 Total plant dry matter (t ha-1) of pre-silking, post-silking, and physiological maturity (R6), the ratio (%) of dry matter accumulation after silking, and harvest index (HI) in different treatments from 2015 to 20161)

Table 3 Effects of planting pattern on dry matter partitioning (g/plant) in different organs at physiological maturity (R6)

Table 4 Effects of planting pattern on 13C-photosynthates distribution in different organs (%) at 24 hours after labelling (24 h) and physiological maturity (R6) in the 2016 growing season

4. Discussion

The main reason for farmers in China to practice intercropping is that it can increase land productivity and profitability (Odhiambo et al. 2011; Feike et al. 2012).Selecting the right crops for intercropping can make good use of resources, thereby increasing the yield per unit area of farmland. In this study, we found that intercropping greatly increased land use efficiency. Previous research on maize/peanut intercropping showed that the LERs of maize/peanut intercropping with different patterns are greater than 1 (Li M et al. 2013; Meng et al. 2016), suggesting a yield advantage and substantially higher land use efficiency,and our findings were consistent with those results. The yield of maize (at the same land area) in the intercropping system was significantly higher than that in the sole cropping system; however, the pod yield of peanut was decreased.A simple calculation can illustrate the economic rationality of intercropping. Thus, the gross economic profit for the intercropping system was 2.56×104CNY ha-1, which is 23.6% higher than SM (2.07×104CNY ha-1) and 17.4%higher than SP (2.18×104CNY ha-1). Thus, the intercropping system can be economically favorable for farmers, but a full evaluation of costs and benefits should also consider differences in costs, e.g., labor cost and mechanical cost.

In terms of grain yield components, the most dramatic responses to planting pattern were observed in KNE,followed by the number of ears of 5-m row and TKW (Fig. 3).Previous studies have found that low-light stress affects the development of reproductive organs and results in seed abortion (Jia et al. 2007; Zhang et al. 2011), whereas increased light may significantly increase the number of kernels per ear and decrease barrenness (Shi et al. 2013).Munz et al. (2014) reported that border row effects on light interception in intercropping are mainly attributed to the decreased shading from nearby plants for the taller component and the increased shading from nearby plant for the shorter component. In our study, we found that intercropping increased the canopy transmittance of maize(Fig. 4), indicating that intercropping can significantly improve the light condition of maize plants. Therefore,we infer that the higher KNE and higher ear number at R6 may have been due to improved light conditions within the canopy, which led to fewer barren stalks than in SM.

Increasing the leaf photosynthetic performance is one of the most important measures for obtaining high yields in summer maize (Liu et al. 2015; Ren et al. 2016). Advantage of intercropping is probably derived from high light use efficiency above-ground and nutrients (e.g., nitrogen (N))below-ground (Lv et al. 2014). In our study, we found that intercropping improved the light condition of ear leaves(Fig. 4), causing the ear leaves of intercropped maize to have greater exposure to sunlight than those of sole maize.Ability to capture sunlight of maize (showed by the increased Pn) was enhanced at border and inner rows compared with SM (Fig. 5). Intercropped legume probably facilitated growth of maize by transferring the N fixed (Li et al. 2009; Li L et al. 2013; White et al. 2013). In addition, Li et al. (2006)and Zhang et al. (2013) reported that intercropped maize proliferated its roots more deeply than sole maize and had a greater root length density (root length per unit soil volume).During the reproductive period of maize, the deeper and longer roots in the intercrop could support better access to the increased available N, which may be the reason for the higher active photosynthetic duration of functional leaves under the intercropping system in this study.

Dry matter accumulation is the material basis of grain formation, and the formation of yield is closely related to its accumulation, distribution, and transfer among various organs (Saidou et al. 2003; Liu 2017). The amount of dry matter accumulation after silking directly determines yield(Tollenaar and Daynard 1982; Sen et al. 2016); moreover,the dry matter distribution and transport in the late growth stage determine the final yield in summer maize. A previous study pointed out that intercropping is beneficial to the accumulation of dry matter in maize ear (Gao 2016). Similar results were observed in our study. Clear increases in total dry matter accumulation at R6 and the ratio of dry matter accumulation after silking were also observed in border and inner rows of IM (Table 2). Jiao et al. (2007) found that intercropping promotes the distribution of photosynthates into the grain and increases the HI (Jiao et al. 2008). This conclusion was confirmed in this study by a13C isotope labelling test. At 24 h, we found that the maximum ratio of distribution of labeled photosynthates occurred in stem, followed by leaf and ear bracts (Table 4). Then,photosynthates were redistributed to the grain during the latter growing period. At physiological maturity, intercropping led to a reduction of13C-photosynthates in stem and leaves and promoted the distribution of13C-photosynthates to grain.We concluded that under the intercropping condition, the improved light conditions, on one hand, decrease barrenness and increased KNE, on the other hand, increased the Pnof ear leaves and prolonged the APD, which promoted the transport of photosynthates to grain.

5. Conclusion

In summary, we found yield advantages and higher land productivity in the maize/peanut intercropping system under a 4:6 pattern (four rows of maize and six rows of peanut)based on LER values in both years. Maize played an important role in determining the yields in the intercropping system; it was the dominant and superior crop and had a stronger ability to obtain resources than peanut when intercropped, especially the border row of intercropped maize. The higher grain yield of IM resulted mainly from the higher KNE at physiological maturity. This increase was essentially attributable to the improved light condition,which enhanced female spike differentiation and reduced seed abortion and barrenness. In addition, intercropping increased the light transmittance ratio, which provided sufficient light conditions for leaf photosynthesis and benefitted grain filling. Likewise, intercropping promoted the total dry matter accumulation, the ratio of accumulation after silking, and the distribution of13C-photosynthates from stem and leaf to grain, resulting in yield increase.

Acknowledgements

We acknowledge the financial support of the National Key Research and Development Program of China(2017YFD0301001), the National Natural Science Foundation of China (31301274 and 31171497), funds from the Shandong “Double Tops” Program, China(SYL2017XTTD14), and the Open Project of State Key Laboratory of Crop Biology in Shandong Agricultural University, China (2018KF10). I also thank my mentor and classmates for their many helpful comments and the reviewers for helping improve the original manuscript.