Xuanxuan Xia?Kexiang Gao?Xianshuang Xing?Rui Yang?Shuyong Zhang?Zilong Du?Jing Guo?Xia Liu

Introduction

Poplar(Populus sp.)is a fast-growing timber tree genus planted widely in northern China(Yang et al.2011).The currently applied multi-generation successive rotation management model for fast-growing and high-yielding poplar plantations can lead to reduced soil fertility and to yield reduction.Many factors contribute to the successive rotation obstacles facing poplar plantation,including rhizosphere soil allelochemicals and deterioration of soil physical and chemical properties.The effect of accumulation of phenolic acids in plantation soils on poplar seedlings is the most important reason for yield reduction(Tan et al.2008).Therefore,it is important to develop treatments to reduce this type of impact in the interest of sustainable development of the timber industry.

Soil microorganisms contribute to maintenance of soil functions,including nutrition cycling and bioremediation(Ye and Thomas 2001),and also benefit the healthy growth of plants(Berg 2009).It is important to maintain high diversity of soil microbes for the sustainable development of agriculture and forestry(Bhat 2013).Fungus fertilizer contains active microbes(Ge et al.2003)that improve nutritional conditions of the plant rhizosphere and inhibit the growth of pathogenic bacteria through release of enzymes and other metabolites.Fugus fertilizer is a type of pollution-free fertilizer.Applying fungus fertilizer can promote plant growth,increase plant yield,improve quality of agricultural products and improve ecological environments(Ge et al.2003).Chaetomium globosum ND35(Ascomycotina,Pyrenomycetes,Sphaeriales,Melanosporaceae)is a dominant endophytic bacteria strain isolated from healthy Populus tomentosa(Gao et al.2011).C.globosum ND35 fungus fertilizer(hereinafter referred to as ND35 fungus fertilizer)can improve the microbial community structure of replanted soil(Liu et al.1999)and can improve soil enzyme activities(Song et al.2015).To date there is inadequate knowledge of the capacity of ND35 fungus fertilizer to improve the physiological and ecological characteristics of plants cropped in successive rotations.In this study,we investigated the effect of ND35 fungus fertilizer on physiological characteristics of I-107 poplar(Populus euramericana cv.‘Zhonglin46’)seedlings in plantation soils.Our objective was to establish a theoretical basis for overcoming the obstacles of successive rotation in poplar plantations.

Materials and methods

Study area

Our study site was located in the Forestry Experimental Station of Shandong Agricultural University(35°38′–36°33′N,116°02′–117°59′E),which has a warm temperate semi-humid continental monsoon climate.The annual mean temperature of the area is 12.9°C,the annual accumulated temperature is about 2350–4777 °C,frost-free days number 202 per year,and annual average precipitation is 741.8 mm,which is concentrated in July–September(Chen et al.2008).Soils are mainly brown soils of pH about 8.4(Liu et al.2010).

Study material and disposal

Soils were sampled at a 2nd generation woodland,Gaoqiao ForestFarm,Ningyang county,Tai’an,China.We cutpoplar twigs of similar size into cuttings of 20 cm in late March 2015 and soaked the cuttings in distilled water.The cuttings were transfered to fresh distilled water every 2 days until they had root primordia,when they were planted into pots in early April.Twenty-one kg ofpotting soilwere used foreach pot(38 cm deep with a diameter of 45 cm).Six dosages of ND35 fungus fertilizer were prepared with 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1for treatments CK,T1,T2,T3,T4,T5,and T6,respectively.The ND35 fungus fertilizer was provided by Professor Gao Kexiang from college of plant protection,Shandong Agricultural University.The effectively live bacteria could reach up to 2.0×108-cfu g-1.Soil without ND35 fungus fertilizer was also prepared as a control treatment(CK).The fungus fertilizer was well mixed with soil and 6 replicates were prepared for each treatment.Plantswere watered every 5 days.In early August 2015,after 4 months of growth in pots,plant physiological indexes were recorded.

Methods

Light response

In August 2015,we selected three robust seedlings of similar size from each treatment to document the parameters of photosynthesis.Three mature leaves in the middle of each test plant were selected and then marked.Using a portable photosynthesis system(CIRAS-2,PPS Co.Ltd.,UK)the photosynthetic parameters were measured three times on each of the marked leaves on sunny days(between 8:30 and 11:00 am)so that nine measurements were made for each seedling.During each measurement,the relative

humidity was maintained at 58±4.0%,CO2concentration was maintained (by a liquid CO2cylinder) at 380 ± 5.0 μmol mol-1,and air temperature of the leaf chamber was maintained at about 26–28 °C.Photosynthetic photon flux density(PPFD)was controlled by a CIRAS-2 LED irradiation source,and the PPFD values were 2000,1500,1000,700,400,200,150,120,100,50,20 and 0 μmol m-2s-1.Parameters including net photosynthetic rate(Pn,μmol m-2s-1),PPFD,transpiration rate(E, mmol m-2s-1), stomatal conductance (Gs,mmol m-2s-1),and intercellular CO2concentration(Ci,μmol mol-1)were automatically recorded by the system.The light-response curves of Pnto PPFD under different soil water conditions were drawn using Excel?.We obtained the apparent quantum yield(Φ,mol mol-1)by the linear regression method of the Pn-PPFD curves under PPFD ≤ 200 μmol m-2s-1(Xu 2002)and maximum net photosynthetic rate(Pnmax)was calculated based on the trend of the measured data points(Lang et al.2013).Instantaneous light use efficiency(LUE)was calculated according to the formula LUE=Pn/PPFD(Long et al.1993).

Chlorophyll fluorescence parameters

Chlorophyll fluorescence parameters were measured simultaneous with light response monitoring and were measured by FMS-2 fluorometer(FMS-2,Hansatech,Britain).Actual photochemical efficiency ΦPSIIand non-photochemical quenching coefficient NPQ were calculated according the following formulas(Rohacek 2002):

where Fm′is the maximum chlorophyll fluorescence yield in the light-adapted state,Fs is steady-state chlorophyll fluorescence yield in the light-adapted state,and Fm is the maximum maximum chlorophyll fluorescence yield in the dark-adapted state.

Chlorophyll content index(ChlNDI)and xanthophyll cycle index(PRI)

These two indices were measured by a spectrometer(PP System).ChlNDI and PRI were calculated according to the formulas(Richardson et al.2002;Stylinski et al.2002;Zhang et al.2007;Gamon et al.1990,1992;Weng et al.2006):

PRI is closely related to the de-epoxidation degree of the xanthophyll cycle.More than 20 leaves were selected from each treatment and every leave was measured at least 4 times,so that there were at least 80 data points for every treatment.

Root vigor was measured according to the triphenyl tetrazolium chloride(TTC)method(μg g-1h-1)(Zou 2006);and nitrate reductase activity(μgwas measured according to Liu Ping(Liu and Li 2007).The height of each poplar seedling was measured for all treatments after the observation of physiological indexes.The total roots,stems,and leaves were first treated at 105°C for 30 min to deactivate enzymes,and then held at 80°C until dry for measuring the dry weight(Fumanal et al.2006).

Statistical analysis

The figures were drawn using Excel 2003 for Windows and statistical analyses were carried out using Statistical Program for Social Sciences(SPSS,Chicago,IL,USA).Differences between means were tested using one-way ANOVA and the least significant difference(LSD)function in SPSS 19.0.The statistical significance level was α=0.05.

Results and analysis

Effects of fungus fertilizer on chlorophyll content index(ChlNDI)of poplar

With increasing fertilizer application,chlorophyll content index(ChlNDI)also increased(Fig.1).Compared with the control,chlorophyll content of T1,T2,T3,T4,T5 and T6 increased 3.5,5.0,8.0,9.9,14.4 and 16.4%,respectively.When fertilizer application was at T3 or higher,the difference was significant,showing that fungus fertilizer promoted the formation of chlorophyll in leaves of poplar.

Effects of fungus fertilizer on net photosynthetic rate(P n)and quantum efficiency(Φ)of poplar

Net photosynthetic rate(Pn)and PPFD increased with increasing application of fertilizer(Fig.2).Under low light intensity (PPFD ＜ 200 μmol m-2s-1), Pninitially increased sharply in a linear trend with increasing PPFD.The rate of increase slowed until under higher light intensity(about PPFD ＞ 1500 μmol m-2s-1),there was little change of Pnwith increasing PPFD.With increasing application of fertilizer,the maximum net photosynthetic rate(Pnmax)initially increased and then decreased(Fig.2a).Pnmaxpeaked at the T3 treatment(0.67 g kg-1)and the relationship of Pnmaxamong the treatments showed T3＞T4＞T5＞T6＞T2＞T1＞CK. For example,compared with CK,Pnof T1,T2,T3,T4,T5 and T6 at PPFD=1500 μmol m-2s-1increased 5.9,14.1,46.3,42.6,37.5 and 26.0%,respectively,all significantly greater than the control mean.The trend of quantum efficiency(Φ)of poplar by treatment was consistent with that of Pnmax(i.e.,increased initially and then decreased).Quantum efficiency at T4(1.0 g)was highest of all treatments(0.0616 mol mol-1)and,compared with CK,Φ of T1～T6 increased by 5.6,10.9,30.9,37.2,25.6 and 20.5%,respectively.This showed that appropriate applications of fungus fertilizer improved the utilization eff iciency of poplar leaves in weak light.

Fig.1 Chlorophyll content index(ChlNDI)of poplar under different treatments.Each bar represents the mean of at least three plants with twenty-seven replicate ChlNDI responses for each treatment.The error bars represent the mean±SE.The same letter on the bar means the character between treatments are not significant at the P＜0.05 level.Dosages of ND35 fungus fertilizer for treatments CK,T1,T2,T3,T4,T5,and T6 were 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1,respectively

Effects of fungus fertilizer on light use efficiency(LUE)

Under different doses of fertilizer,light use efficiency(LUE)of all treatments showed similar trends with increasing PPFD (Fig.3).LUE rose rapidly when PPFD ＜ 200 μmol m-2s-1while it decreased slowly at PPFD ＞ 200 μmol m-2s-1.LUE was high when PPFD ranged from 100 to 700 μmol m-2s-1in all treatments.LUE levels of all groups treated with fungus fertilizer were higher than LUE of the control group.In descending rank order,LUE levels by treatment were T3＞T4＞T5＞T6＞T2＞T1＞CK.This showed that fungus fertilizer(0.67–1.67 g)improved the light use efficiency of poplar leaves.

Effects of fungus fertilizer on chlorophyll fluorescence parameters

Non-photochemical quenching(NPQ)levels at fertilizer applications T1–T6 were higher than at CK,and the change trend of NPQ for all groups initially decreased and then increased with the increase of fungus fertilizer content(Fig.4a).NPQ peaked at treatment T3(0.67 g kg-1).NPQ was similar for treatments T1 and CK but treatments T2–T6 yielded NPQ levels significantly lower than the mean level for CK.Under different treatments,both actual photochemical efficiency of PSII(ΦPSII)and electron transport rate(ETR)were higher than mean control levels(Fig.4b,c)Mean ΦPSIIand ETR levels were significantly higher for all treatments than for the control.The trends for both ΦPSIIand ETR initially increased and then decreased,peaking at T3(0.67 g kg-1).Compared with CK,ETR values for treatments T1～T6 increased by 6.6,12.7,67.8,44.1,20.0 and 47.8%,respectively.The relationship between Pnmaxand ETR was fitted to a third degree polynomial function(Fig.4d)as follows:

Fig.2 Net photosynthetic rate(Pn)and quantum efficiency(Φ)of poplar under different treatments.a Each point represents the mean of at least three plants with twenty-seven replicate Pnresponses for each light point.The lines are fitted to the response of Pnto time under different treatments.b Each bar represents the replicate Φ responses for each treatment.The same letter on the bar means the character between treatments are not significant at the P＜0.05 level.The error bars represent the mean±SE.Dosages of ND35 fungus fertilizer for treatments CK,T1,T2,T3,T4,T5,and T6 were 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1,respectively

Fig.3 Light use efficiency(LUE)of poplar under different treatments.Each point represents the mean of at least three plants with twenty-seven replicate LUE responses for each light point.The lines are fitted to the response of LUE to light under different treatments.Dosages of ND35 fungus fertilizer for treatments CK,T1,T2,T3,T4,T5,and T6 were 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1,respectively

Effects of fungus fertilizer on xanthophyll cycle index(PRI)

The xanthophyll cycle index(PRI)of poplar leaves increased with increasing fertilizer application(Fig.5),and T1～T6 increased by 10.6,43.4,53.7,71.0,104.2 and 111.5%,respectively.Except for the T1 treatment,the PRI values of all treatment groups were significantly greater than that of CK.In view of the negative correlation between PRI and the extent of de-epoxidation of the xanthophyll cycle(Peng et al.2009),we expected that the de-epoxidation extent of the xanthophyll cycle would decline after fertilization.The increasing of concentration fungus fertilizer in the soil reduced the de-epoxidation extent of xanthophyll cycle of poplar leaves,i.e.,the excess light energy dissipated through xanthophyll cycle was indeed reduced.

Fig.4 Chlorophyll fluorescence parameters of poplar by fertilizer treatment.Each bar represents the mean of at least three plants with twenty-seven replicate non-photochemical quenching,actual photochemical efficiency of PSII and electron transport rate responses for each treatment.The same letter on the bar means the character between treatments are not significant at the P＜0.05 level.The error bars represent the mean±SE.The lines are fitted to the response of Pnmaxto electron transport rate under different treatments.Dosages of ND35 fungus fertilizer for treatments CK,T1,T2,T3,T4,T5,and T6 were 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1,respectively

Fig.5 Xanthophyll cycle index(PRI)of poplar by fertilizer treatment.Each bar represents the replicate xanthophyll cycle index responses for each treatment.The same letter on the bar means the character between treatments are not significant at the P＜0.05 level.The error bars represent the mean±SE.Dosages of ND35 fungus fertilizer for treatments CK,T1,T2,T3,T4,T5,and T6 were 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1,respectively

Effects of fungus fertilizer on nitrate reductase(NR)activity and root vigor

Nitrate reductase(NR)activity and root vigor initially increased and then decreased with increasing application of fungus fertilizer(Fig.6).NR activity peaked(1.78 μg NO2-g-1h-1)at treatment T3(0.67 g kg-1),showing an increase of 80.1%compared to CK.When fungus fertilizer content in the soil exceeded 1.0 g kg-1(T4),NR activity declined with increasing fungus fertilizer application.NR activity of T6 treatment was the lowest of all treatments and was similar to that of CK.Root vigor of T3 and T4 treatments(0.67–1.0 g kg-1)was highest.Root vigor at all fertilizer treatment levels was significantly higher than that of the control.

With increasing fungus fertilizer content,both plant height and biomass of leaves,stems and roots initially increased and then decreased(Table 1).Plant morphology parameters peaked at treatment T3.

Conclusion and discussion

Fig.6 Nitrate reductase(NR)activity and root vigor of poplar by fertilizer treatment.Each bar represents the replicate nitrate reductase activity and root vigor responses for each treatment.The same letter on the bar means the character between treatments are not significant at the P＜0.05 level.The error bars represent the mean±SE.Dosages of ND35 fungus fertilizer for treatments CK,T1,T2,T3,T4,T5,and T6 were 0,0.17,0.33,0.67,1.00,1.33 and 1.67 g kg-1,respectively

Table 1 Plant height and biomass of poplar under different treatments

When C.globosum ND35 infects the roots of poplar seedlings,the mycelium mainly intrudes into the intercellular space(Meng et al.2009).Our research showed that applying fungus fertilizer improved root vigor of poplar seedlings.Of the treatment groups,treatments T3 and T4(0.67–1.0 g kg-1)proved superior(Fig.6).These levels of fertilization enhanced absorption capacity,synthesis ability,oxidation ability and reduction ability.Aerial parts of seedings rely on the water and fertilizer absorbed by underground parts,and on amino acids and some growth substances produced by underground parts.Both plant height and biomass of leaves,stems,and roots initially were affected(Table 1).Pnmaxand Φ of T3 and T4(0.67–1.0 g kg-1)were at high levels,meaning that the operating state of the photosynthetic apparatus was improved and the capacity for absorption,conversion and utilization of weak light was enhanced(Xia et al.2014).Application of appropriate amounts of fungus fertilizer promoted root vigor and then improved use ability in weak light,indicating that fungus fertilizer helped to improve the operating states of photosynthetic apparatus and photosynthetic efficiency of poplar leaves as reported by Xia et al.(2014).This also enhanced the accumulation of dry matter by the seedlings(Table 1).

Nitrogen plays a core role in the process of plant metabolism,growth,reproduction and genetics(Chaukiyal et al.2014).Nitrate reductase(NR),which regulates and controls the assimilation of primary nitrogen,is an important regulatory enzyme in the process of nitrogen metabolism of plants(Catarina et al.2013).It plays a catalytic role in the nitrate nitrosation process,which is closely related to the biological metabolism,photosynthesis and the signal transduction of various cells.Nitrate reductase activity was positively correlated with nitrogen metabolism,and it is commonly used to represent the strength of nitrogen metabolism.In this study,NR activity of treatments T2–T5(0.33–1.33 g kg-1)increased signif icantly over that of the control.This shows that appropriate amounts of fungus fertilizer increased NR activity,which enhanced plant nitrogen metabolism.Higher NR activity can improve plant resistance to disease and pests(Rimaljeet et al.2014)but this was not tested in our study.

Varying content of chlorophyll can reflect variation in physiological states of plants(Sims and Gamon 2002).In this study,increasing applications of fungus fertilizer yielded increasing levels of chlorophyll content(Fig.1).This would be expected to enhance performance of the photosynthetic apparatus by increasing absorption,transmission and conversion of light energy.Li et al.(2014)reported that chlorophyll content varied with application level of mixed fungus fertilizer.Li et al.(2012)reported that three kinds of fungus fertilizer(Lianchawang,Hugenbao and Trichoderma microbial fertilizers)had no significant effect on chlorophyll and carotenoid content.The photosynthesis of plants is influenced by environmental factors and physiological characteristics(Xia et al.2015).The rate of photosynthesis is related to chlorophyll content,but is more closely related to PRI and intercellular CO2concentration(Ci)(Stylinski et al.2002).In this study,high levels of fungus fertilizer content(T5 and T6)led to declining Pnmaxand Φ,possibly due to impacts of the xanthophyll cycle or Ci.This topic requires further study.

Non-photochemical quenching(NPQ)and xanthophyll cycle,which are energy dissipated in the form of heat,are the main way of dissipating excess light energy for higher plants.The three components of the xanthophyll cycle,viz.violaxanthin(V),antheraxanthin(A)and zeaxanthin(Z),transform reciprocally in accordance with surplus levels of light energy(Sun et al.2006).When light energy absorbed by the plant is in surplus,double epoxy V transforms from single epoxy A into free epoxy Z(i.e.,V→A→Z),while this transformation proceeds in the opposite direction in the dark(Meng and Gao 2011).The formula(A+Z)/(V+A+Z)(i.e.,PRI)represents the de-epoxidation extent of the xanthophyll cycle.PRI is associated with the de-epoxidation state of the xanthophyll cycle which is involved in nonphotochemical heat dissipation(Dobrowski et al.2005).We found that PRI increased with increasing levels of ND35 fungus fertilizer content in replanted soil.But NPQ of CK-T3 declined,showing consistency with the trends of(A+Z)/(V+A+Z).The electron transport rate(ETR)increased with increasing fertilization,showing that the photosynthetic apparatus of poplar distributed more light energy for photosynthesis(Pnmaxand Φ increased)and thus the surplus of light energy decreased.This increased the utilization efficiency of solar energy to a certain extent(Fig.3).NPQ increased in treatments T4–T6(1.0–1.67 g kg-1)but remained lower than at T2.ETR trended downward,indicating that the light use efficiency of the photosynthetic apparatus declined somewhat with increasing fertilizer application.We fitted the relationship between Pnmaxand ETR to a third degree polynomial function(Fig.4d).

In conclusion,the application of fungus fertilizer positively influenced root vigor,nitrate reductase activity,electron transport rate,and various photosynthetic parameters.Applying 0.67–1.0 g fungus fertilizer per kg of plantation soil proved the optimum application rate for reducing adverse impacts on soils of successive rotations of poplar plantation.

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