A pH-responsivesustained release nitrogen fertilizer hydrogel based on aminated cellulose nanofibercationic copolymer for application in irrigated neutral soils

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Journal of Cleaner Production 368 (2022) 133098
Available online 18 July 2022
0959-6526/© 2022 Elsevier Ltd. All rights reserved.
A pH-responsive/sustained release nitrogen fertilizer hydrogel based on 
aminated cellulose nanofiber/cationic copolymer for application in 
irrigated neutral soils 
Hiba Shaghaleh a,1, Yousef Alhaj Hamoud b,1, Xu Xu a,*, Shifa Wang a,**, He Liu c 
a College of Chemical Engineering, Jiangsu Provincial Key Lab for the Chemistry and Utilization of Agro-forest Biomass, Co-Innovation Center of Efficient Processing and 
Utilization of Forest Resources, Jiangsu Key Lab of Biomass-based Green Fuels and Chemicals, Nanjing Forestry University, Nanjing, 210037, China 
b College of Agricultural Science and Engineering, Hohai University, Nanjing, 210098, China 
c Institute of Chemical Industry of Forestry Products, Chinese Academy of Forestry, Key Laboratory of Biomass Energy and Material, National Engineering Laboratory for 
Biomass Chemical Utilization, Key and Open Laboratory of Forest Chemical Engineering, State Forestry Administration, Nanjing, 210042, Jiangsu Province, China 
A R T I C L E I N F O 
Handling Editor: M.T. Moreira 
Keywords: 
pH-responsive release fertilizer hydrogel 
Aminated nanofibrillated cellulose 
Sustained-release mechanisms 
Neutral soil 
Biodegradability 
Nitrogen use efficiency 
A B S T R A C T 
Stimuli-responsive release nitrogen (N)-fertilizer hydrogels are new materials recently introduced to improve 
control and sustained release N-fertilizer hydrogels efficacy by adding additional functionality for greater N use 
efficiency. However, the stimuli-responsive behavior and release mechanisms of these fertilizer hydrogels in 
response to irrigated-soil stimulus fluctuations during different plant growth stages are still facing limitations and 
have not been considered. Herein, a novel N-fertilizer nanocomposite hydrogel with the function of N pH- 
responsive/sustained release (pHRSRNFH) was prepared based on wheat straw aminated-cellulose nanofibers 
(A-CNFs) and cationic poly(acrylamide-co-2-aminoethyl methacrylate hydrochloride) (PAM-PAEM) by direct 
ammonium nitrate (AN) fertilizer encapsulation. The fertilizer hydrogel structure, properties, and effects on N 
use efficiency and N metabolism process were characterized by FTIR, zeta potential, SEM, porosity, swelling- 
release behaviors, TEM, flowcytometric analysis, and N use efficiency indicators. The hydrogel nanocomposite 
with 3 wt% A-CNFs and 4 wt% AEM (pHRSRNFH4) exhibited desirable enhancement of characterizations, pH- 
responsive/sustained behaviors, and biodegradability. The soil and buffers release kinetic studies in-vitro 
revealed the best pH-dependent/sustained AN release of 3.00 and 2.69 mg.day− 1 at pH 5.5 and 0.92 and 0.55 
mg.day− 1 at pH 7.4 from 1g pHRSRNFH4 for 58 and 65 days, respectively, desirably synchronizing with the pH 
fluctuations of irrigated-neutral soil. The whole lifetime of AN release data revealed that the three sustained 
delivery stages were governed by the First-order mechanism, followed by Zeroth-order, and finally via the 
Higuchi mechanism, covering the N crop requirements during different plant growth phases. Application of 
pHRSRNFH4 at 1 g kg− 1 irrigated-neutral soil successfully improved water-holding capacity and N recovery ef-
ficiency by 15.7% and 38.6%, respectively, compared with free AN treated soil with over 90-days sustained AN 
release. Furthermore, positive impacts on rice growth indicators, N-nutrition status, and cell progression were 
achieved with a feasible-compatible application, demonstrating its further significant potential to be a viable 
alternative fertilizer formulation for N/water management of cropping systems in the irrigated-neutral soils. 
1. Introduction 
Agriculture is now facing the challenge of water scarcity, food se-
curity, and environmental sustainability, which are adversely affected 
by the inefficient input of water and fertilizers (Mateo-Sagasta et al., 
2017; Rosa et al., 2020). Nitrogen (N) is the most essential plant 
nutrient, and N-fertilizers are widely applied, playing a vital role in 
agricultural productivity and quality in most agricultural cropping sys-
tems (Maheswari et al., 2017). Globally, agricultural production has 
improved over the last 50 years due to the excessive enlargement in 
N-fertilizer inputs which increased by 800%, of which 35% is used in 
* Corresponding author. 
** Corresponding author. Longpan Road, Nanjing, 210042, Jiangsu Province, China. 
E-mail addresses: xuxu200121@hotmail.com (X. Xu), WSfyyq@njfu.com.cn (S. Wang). 
1 These authors contributed equally to this work. 
Contents lists available at ScienceDirect 
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https://doi.org/10.1016/j.jclepro.2022.133098 
Received 14 January 2022; Received in revised form 9 June 2022; Accepted 8 July 2022 
mailto:xuxu200121@hotmail.com
mailto:WSfyyq@njfu.com.cn
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2
China (Zhang et al., 2014). However, further increases in N-fertilizer 
consumption are unlikely to be effective in increasing crop yields as 
50–70% of the conventionally delivered N-fertilizers are lost into the 
environment via volatilization, denitrification, and leaching, leading to 
severe environmental pollution, and low nitrogen use efficiency (NUE) 
(Zhou et al., 2018). Therefore, there is an urgent need to develop new 
N-fertilization techniques in an appropriate and timely supply manner 
that consistently matches high yield production and significant N utili-
zation for sustainable crop production. 
Intensive accomplishments in fertilizers production technologies 
have been introduced to improve fertilizer use efficiency by reducing 
fertilizer application rate and increasing plant productivity. Thus, fer-
tilizer immobilization, coating, or encapsulation into controlled-release 
fertilizer systems (CRFs) based on natural/synthetic polymeric materials 
have been introduced to allow a slow nutrient release to be better co-
ordinated with the plant life cycle with less nutrient loss, improving 
fertilizer use efficiency while reducing environmental risk (Zhou et al., 
2018; Rop et al., 2018). However, the vulnerability of CRFs to response 
to soil stimulus fluctuations of soil pH, soil moisture contents, and plant 
root activity can significantly affect the fertilizer release rate and pre-
vent matching plant-nutrient demands during the critical growth pe-
riods. Moreover, the feasibility, long-term active quality, and 
degradability of CRFs are still demanding challenges. 
Alternatively, fertilizer embedded into stimuli-responsive materials 
that can alter their release behavior in response to surrounding soil 
fluctuations have the potential to provide an efficient fertilizer delivery 
that precisely synchronizes with plant nutrients demand in proper 
quantity and optimal time. Yet, very few attempts to innovate stimuli- 
responsive release fertilizer systems based on different polymeric ma-
terials have been recently made, i.e., poly(N, N-dimethylaminoethyl 
methacrylate)/polydopamine/H4NO4PZn composite, methylcellulose/ 
hydroxypropyl/methylcellulose/K2SO4 hydrogel, nanocellulose/so-
dium alginate/MOF hydrogel, and TEMPO-oxidized nanocellulose/MOF 
hydrogel composites (Feng et al., 2015; Chen and Chen, 2019; Wang 
et al., 2021; Lin et al., 2021). Hydrogels play an astonishing role in the 
fabrication of such a new branch of fertilizer materials and the elder 
CRFs generation due to their restricted 3D hygroscopic multidimen-
sional network structure, retaining a large amount of water/liquid fer-
tilizerat 
affordable cost, providing high-quality N/wter management approaches 
supporting environment-agriculture sustainably. 
CRediT authorship contribution statement 
Hiba Shaghaleh: Conceptualization, Methodology, Data curation, 
Software, Writing – original draft, Writing – review & editing. Yousef 
Alhaj Hamoud: Conceptualization, Methodology, Data curation, Soft-
ware, Writing – original draft, Writing – review & editing. Xu Xu: 
Visualization, Supervision, Validation, Writing – review & editing. Shifa 
Wang: Visualization, Supervision, Validation, Writing – review & edit-
ing. He Liu: Visualization, Supervision, Validation, Writing – review & 
editing. 
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 Major Program of the National 
Natural Science Foundation of China (Grant No.31890774), the Opening 
Fig. 7. (a) Percentages of mass loss of PHRSRNFH4 and CRNFH and related in-vivo biodegradation rate as a function of application time and hydrogel formulation. (b) 
are SEM micrographs showing physical/chemical biodegradation after 1 (I), 2 (II), 3 (III) months of incubation and (IV) optical graphs after 3 months’ incubation of 
PHRSRNFH4 and CRNFH, respectively. 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
15
Project of Guangxi Key Laboratory of Forest Products Chemistry and 
Engineering (GXFK2008), the Top-notch Academic Programs Project of 
the Jiangsu Higher Education Institutions (ATPP), and the Priority Ac-
ademic Program Development of the Jiangsu Higher Education In-
stitutions (PAPD). 
Appendix A. Supplementary data 
Supplementary data to this article can be found online at https://doi. 
org/10.1016/j.jclepro.2022.133098. 
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	A pH-responsive/sustained release nitrogen fertilizer hydrogel based on aminated cellulose nanofiber/cationic copolymer for ...
	1 Introduction
	2 Experimental section
	2.1 Material
	2.2 A-CNFs production from WS
	2.3 Fabrication of AN-loaded A-CNF/PAM-PAEM hydrogels for pH-responsive/sustained AN fertilizer delivery
	2.4 Characterization
	2.5 Water uptake capacity (S) of fertilizer hydrogel and water holding capacity (WHC) in soil
	2.6 In-vitro AN release kinetic studying of AN fertilizer hydrogel formulations
	2.7 Greenhouse pot trials with pHRSRNFH-based responsive/sustained AN delivery system
	2.7.1 Experimental site and design
	2.7.2 An release kinetic in the irrigated soil, plant, and N efficiency indicators with rice model
	2.7.3 Biodegradation testing
	2.8 pHRSRNFH feasibility
	2.9 Statistical analysis
	3 Results and discussion
	3.1 Synthesis and characterization
	3.2 Surface morphology
	3.3 In-vitro AN kinetic release of fertilizer hydrogel formulations
	3.4 AN release in the irrigated-neutral soil cultivated with rice under the greenhouse conditions
	3.5 The effects of PHRSRNFH4 application on the Nnutrition status, cell ultrastructure, cell cycle progression, and efficien ...
	3.6 The biodegradability and feasibility evaluation of PHRSRNFH4
	4 Conclusions
	CRediT authorship contribution statement
	Declaration of competing interest
	Acknowledgments
	Appendix A Supplementary data
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gated. In addition, detailed knowledge on how their sustained release 
mechanisms synchronize with nutrient plant demands at the different 
critical growth stages is still largely scarce. Four key factors inform the 
adaption of smart/steady fertilizer hydrogel systems: (1) the system 
sensing interfaces including soil/root signals, (2) the 
stimulus-responsive release behavior of the adapted system against 
these signals and plant growth stages, (3) system biodegradability, and 
(4) feasibility, all of which need to be considered. 
Regarding the sensing interfaces, it has been observed that soil 
drying/re-wetting cycles during water-saving irrigation have a sche-
matic impact on pH soil property resulting in a relatively dramatic 
change in soil pH environment according to soil pH category (Alhaj 
Hamoud et al., 2019). Mainly, in the neutral soils, with an initial pH ≥
6.5 up to pH of 7.5, the soil pH in the plant root zone decreases linearly 
by more than 1 unit during the wetting shifts and shows the opposite 
pattern in the drying shifts under short-term cropping conditions (Ding 
et al., 2019). Besides, the plant roots are highly motivated during the 
re-wetting shifts, producing a high organic acids rate, thus, increasing 
the plant root zone acidity 0.3–0.9 times. Such changes in soil pH values 
can be potentially employed as sensing interfaces to switch on/off the 
pH-responsive fertilizer hydrogel device. In practice, alternate wetting 
and drying (AWD) irrigation, a commonly applied water-saving tech-
nique, can lead to considerable changes in soil pH patterns (Alhaj 
Hamoud et al., 2019). Rice (Oryza sativa. L) is a water-intensive food 
crop, feeding over 40% of the global population (Datta et al., 2017), 
which is threatened by the inefficient use of fertilizer and water; thus, 
AWD-irrigated rice cropping systems have been widely implemented to 
cope with water scarcity (Alhaj Hamoud et al., 2019). However, the 
lower yields resulting from greater N-volatilization/leaching loss and 
lower water availability under AWD irrigation compared to the 
flooded-rice cropping systems is still the key challenge in ensuring food 
security and environmental sustainability (Materu et al., 2018). There-
fore, the fabrication of a pH-responsive/sustained release N-fertilizer 
hydrogel (pHRSRNFH) system fits the variable pH-stimulus in the 
irrigated-neutral soils under AWD irrigation during different tempera-
tures growth phases of the rice crop as a model is urgently required. 
Regarding the adapted hydrogel material, a platform of PAM which 
is the most commercially common approved soil conditioner and 
structure stabilizing agent with an application rate of 1–20 kg/ha and 
900-18,000 tons/year (Levy and Warrington, 2015; Xiong et al., 2018), 
has been chosen. A cationic-modified food-grade PAM with a viable 
vinyl monomer of 2-aminoethyl methacrylate hydrochloride (AEM) 
holding a primary amine is a suitable positively charged surface prep-
aration. This cationic copolymer could be adsorbed easily onto nega-
tively charged clays in the soil (Xiong et al., 2018) and potentially 
Abbreviations 
A-CNFs Aminated-cellulose nanofibers 
AM Acrylamide 
AEM 2-aminoethyl methacrylate hydrochloride 
A-CNF/PAM-PAEM A-CNFs/cationic poly(AM-co-AEM)-based 
hydrogel 
AN N-fertilizer ammonium nitrate 
ANA-CNF/PAM-PAEM AN-loaded A-CNF/PAM-PAEM hydrogel 
(pHRSRNFH) 
pHRSRNFH pH-responsive/sustained release AN fertilizer hydrogel 
CRNFH Control release AN-fertilizer Hydrogel (AN-loaded PAM) 
TPAP Two-phase air plasma pretreatment approach 
WS Wheat straw 
WSFs Wheat straw fibers 
WSCFs Wheat straw cellulosic fibers 
FTIR Fourier transform infrared spectroscopy 
FESEM Field emission scanning electrons 
BET Brunauer-Emmett-Teller surface area analysis 
AWD Alternate wetting and drying 
NUE Nitrogen use efficiency 
TEM Transmission electron microscope 
WHC Water holding capacity 
Qt Cumulative percentage AN release as a function of time 
k Kinetic constant related to the release rate 
RD Root diameter (cm) 
RWD Root weight density (g.cm− 3) 
NCR Nitrogen crop removal (mg.plant− 1) 
NAG and NAS Nitrogen accumulation in grain and straw (g) 
DWG and DWS Dry weight of the grain and straw (g) 
NCG and NCS Nitrogen content in the grain and straw (%) 
ANRE Apparent nitrogen recovery efficiency (%) 
PFPN Partial factor productivity of nitrogen (g.g− 1) 
NHI Nitrogen harvest index (%) 
NI Nitrogen input (mg.soil− 1) 
GY Grain yield (g.plant− 1) 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
3
introduce preferred release behavior in response to neutral soil pH sig-
nals withHydrochlo-
ride (EDC-HCl), N-hydroxysuccinimide (NHS), 1,4 diaminobutane, 2- 
aminoethyl methacrylate hydrochloride (AEM, 99%), 2-2′-azobis-(2- 
amidinopropane hydrochloride) (V50), N, N-methylene bisacrylamide 
(MBA), 1, 2-di (dimethylamino) ethane (TMEDA, 99%), phosphate- 
buffered saline (PBS), potassium dihydrogen phosphate (KH2PO4, 
≥89%), NaOH, HCL, methanol, and food-grade acrylamide (AM, 99%) 
were obtained from Sinopharm Chemical Reagent Co Ltd. In all exper-
iments, deionized water was used. Soil cores were collected from 
Nanjing, Jiangsu (31◦53′05.5′′N, 118◦51′42.1′′E). 
2.2. A-CNFs production from WS 
For efficient, feasible, and green A-CNFs production with high amino 
substation degree (DSNH2) of free terminal amino-decorated surface, a 
three-step TPAP pretreatment which is followed by TEMPO-oxidation 
free-amine protecting amidation of WS has been applied according to 
our previous work (Shaghaleh et al., 2021). Briefly, 90s-air plasma 
activation using dielectric barrier discharge plasma reactor step-wisely 
occurred through two phases on the WS fibers (WSFs) and subse-
quently on WS cellulosic fibers (WSCFs), combined with mild NaOH 
pretreatment (Fig. 1). The TEMPO-oxidation was carried out by the 
desperation of 5 g of the obtained pretreated WSCF powder, 0.075 g of 
TEMPO, and 0.5 g of Na Br in 1-L deionized water at 1% (w/v), initiated 
by adding 12%, 5 mmol/g o.d.p NaClO solution at 25 ◦C with stirring at 
10 pH until no further decrease in pH was observed. The oxidized sub-
strate was then homogenized to obtain TO-CNFs. To prepare A-CNFs, the 
resulting TO-CNF suspension (4.88 g, carboxyl substation degree 
(DSCOOH) = 1.02, 2.55 mmol COO− /g) was sonicated with MES buffer 
(150 mL, pH = 5.5) for 20 min, then mixed with EDC-HCl (4.8 g, 24.88 
mmol) and NHS (2.86 g, 24.88 mmol) and stirred at 25 ◦C for 15 min. 1, 
4-Diaminobutane (1.62 g, 37.32 mmol) was finally added, and the 
mixture was stirred for 24 h at room temperature. The mixture was 
dialyzed against saturated sodium chloride solution for 24 h and then 
deionized water until no more free diamines were detected in the dial-
ysate. Purified A-CNFs were obtained by freeze-drying. Millipore 
deionized water from the Millipore Milli-Q system (>18 M Ω cm; Merck, 
Darmstadt, Germany) was prepared for the diluted samples. 
2.3. Fabrication of AN-loaded A-CNF/PAM-PAEM hydrogels for pH- 
responsive/sustained AN fertilizer delivery 
A series of physically entrapped A-CNF-based hydrogels were syn-
thesized via typical in situ radical copolymerization in the water of 10% 
wt food-grade AM solution with variable mass ratios of 0.5 %wt AEM 
monomer solution around 1%wt A-CNF nanofiller suspension relative to 
AM amount as expressed in Table 1. The mixture was then stirred at 
room temperature under a nitrogen environment and vigorous stirring 
until homogenous. The NH4NO3 (AN) fertilizer-encapsulated hydrogel 
samples (CRNFH and pHRSRNFH) were prepared by adding 25%wt of 
the total mixture solution of dissolved 0.5 %wt AN solution into the 
prepared A-CNF/AM/AEM mixture before crosslinking reactions with 
10 mg of MBA as a cross-linker agent. The solution was stirred at 250 
rpm for 30 min with a nitrogen purge to eliminate oxygen at 40 ◦C. Then 
0.2 mL of KPS aqueous solution (16 mg/mL) and 0.5 mL of an aqueous 
solution of V50 (16.28 mg/mL) were added as the initiators with 0.045 
mL of TEMED as an accelerator to start the copolymerization. The 
copolymerization was allowed to continue up to 12 h at 40 ◦C and 
maintained under an inert atmosphere before the stirring was stopped. 
The resultant hydrogel precursor solutions were cast at regular PVC pans 
to form dry weight granular hydrogels (1g). Synthesis steps and condi-
tions are shown in Fig. 1 and Table 1. The freshly prepared fertilizer 
hydrogel granules were left overnight at room conditions and purified 
by washing several times with deionized water to remove unreacted 
chemical residues. After that, a part of the wet hydrogel samples was 
centrifuged and then rapidly frozen in a freezer at about − 30 ◦C for 12 h, 
which were then transferred to a freeze-dryer (Free-Zone plus 2.5 L, 
Labconco, Kansas, MO, USA) at a temperature of − 50 ◦C and freeze- 
dried for 5 days. These fully freeze-dried hydrogels were used for 
FTIR, zeta potential, SEM observation, swelling ratios, and water hold-
ing capacity experiments. The other part of purified hydrogel granules 
was dried in a vacuum oven at 30 ◦C before incubation in buffers and soil 
for the kinetic release in vitro and greenhouse pot trial studies. The 
unloaded AN in the supernatant was concentrated to 1 mL using a rotary 
vacuum evaporator and quantified spectrophotometrically at 305 nm. 
AN encapsulation efficiency (EE, w/w%) is calculated using the 
following equation, 
EE ​ = ​
WE
WT
​ × ​ 100 (1) 
Where, WE is the amount of entrapped AN in the hydrogel, and WT is the 
theoretical weight of AN added during preparation. 
2.4. Characterization 
The morphological structure of the prepared A-CNFs was studied by 
atomic force microscopy (AFM, Bruker, Santa Barbara, CA, USA). The 
carboxyl/amine group contents and the relative degree of substitution of 
TO-CNFs (DSCOOH) and A-CNF (DSNH2) surfaces during A-CNFs pro-
duction steps were determined according to our previous study (Sha-
ghaleh et al., 2021), seeing the supportive information. The surface and 
cross-section morphology of the as-prepared fertilizer hydrogels before 
and after their application was observed using field emission scanning 
electrons (FESEM, Hitachi S-4800, Japan). For SEM observation, 
Table 1 
The feed composition ratios of the synthesized AN-fertilizer hydrogel formulations, their related codes, Brunauer-Emmett-Teller (BET) surface area, and AN encap-
sulation efficiency. 
Fertilizer hydrogelsa Code AM (mL)b AEM(mL) A-CNF (mL) AN (%)c Surface area (m2.g− 1) EE (w/w%) 
ANPAM CRNFH 10 0 0 25 44.05 75.2 
ANPAM-PAEM4 
pHRSRNFH1 10 1 0 25 86.48 83.6 
ANA-CNF3/PAM pHRSRNFH2 10 0 0.45 25 93.27 88.1 
ANA-CNF3/PAM-PAEM2.5 
pHRSRNFH3 10 0.5 0.45 25 186.62 94.4 
ANA-CNF3/PAM-PAEM4 
pHRSRNFH4 10 1 0.45 25 213.05 99.9 
ANA-CNF1.5/PAM-PAEM4 
pHRSRNFH5 10 1 0.225 25 138.11 90.6 
a The letters n and m of A-CNFm and AEMn represent the wight ratios (wt%) of AEM and A-CNF relative to AM monomer amount. 
b 10 wt%, 0.5 wt%, and 1 wt% of AM, AEM, and A-CNF (DS = 1.42) solutions were used, respectively. 
c The wt% of NA is relative to the total prepared A-CNF/AM/AEM pre-gel mixture solution amount. AN fertilizer solution was prepared by dissolving 50 g of NH4NO3 
to make a 100 ml aqueous solution. 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
5
hydrogel samples were cut into slices, frozen using liquid nitrogen, 
transferred into a vacuum freeze drier for dehydration, and finally 
spray-coated with gold using a Fine Coat Ion Sputter JFC-1100. Pore 
diameters and the BET surface areas were determined by N2, adsorp-
tion/desorption method (Micromeritics ASAP2020 HD88, USA). Varia-
tions in the surface functional groups and structural properties 
A-CNF/PAM-PAEM hydrogels were identified by a Nicolet 6700 FTIR 
spectrophotometer (Thermo Scientific, USA) at every production/syn-
thesis stage. Zeta potential analysis of A-CNFs, A-CNF/PAM-PAEM, and 
ANA-CNF/PAM-PAEM hydrogels were measured using Zetasizer Nano ZS 
Malvern instruments at 25 ◦C for different pH values. 
2.5. Water uptake capacity (S) of fertilizer hydrogel and water holding 
capacity (WHC) in soil 
For S investigation, 0.1 g (Wd) of dry hydrogel sample was entirely 
immersed into 100 mL of deionized water at 25 ◦C, removed at regular 
time intervals, wiped superficially with filter paper, and weighted (Ws). 
The percentage of maximum swellingat equilibrium (S, %) was 
measured gravimetrically by the following equation: 
S ​ = (Ws − Wd)
Wd
× ​ 100 (2) 
The efficiency of hydrogel to retain water in soil was expressed using 
a WHC indicator a 10 g of dried fertilizer hydrogel was mixed separately 
with 10 kg of dried field soil, placed in an enabled water filtration-PVC 
tube with 200 mesh nylon led, weighed (m1), and followed by slow 
watering from the top of the tube until water passed down through the 
soil from the tube bottom. After water percolation stopped, the weight of 
the loaded tube with the mixture was labeled (m2). The wight of pure 
dried soil was used as control (m0). The WHC (%) of the samples was 
calculated using the following equation: 
WHC ​ =(m2 − m1)
m1
× ​ 100 (3) 
2.6. In-vitro AN release kinetic studying of AN fertilizer hydrogel 
formulations 
For in-vitro AN release experiments, the release kinetics from the 
different AN-entrapped fertilizer hydrogel formulations were assessed in 
60 days laboratory test systems with PBS buffer solutions and soils at 
25 ◦C as a function of varying pH levels applied of pH 5.5 and 7.4. To 
determine the AN release in the buffer solutions, 1 mL of the soaking 
solution samples were collected at predetermined time intervals and 
analyzed for total N content by converting NH4–N and NO3–N forms 
resulting from AN release to NH4–N state using the micro-Kjeldahl 
method (Sparks et al., 2020). To investigate AN release in soil, 8 g of 
each fertilizer hydrogel was buried in 10 kg of field soils with pH 5.5 and 
7.4 at a depth of approximately 10–15 cm below the soil surface. The 
percentages of AN released in the soil were quantified after the specified 
intervals using the micro-Kjeldahl method (Sparks et al., 2020), which 
indicates the total N content presented in the soil resulting from AN 
release in both ammonium and nitrate forms. Organic N in soil was 
omitted. The results were presented in terms of cumulative percentage 
AN release as a function of time ( ​ Qt, %) using the following formula: 
​ Qt =
Mt
M∞
× ​ 100 (4) 
Where, Mt is the cumulative amount of AN released from the fertilizer 
hydrogel formulation at time t, and M∞ is the total amount of AN loaded 
into the hydrogel released at the infinite time. 
Mathematical modeling was performed to characterize the 
sustained/pH-dependent AN release kinetics from CRNFH and 
pHRSRNFH4 formulations as a function of pH at a time and assay how 
they match N plant requirements during the growing season. The release 
profiles of CRNFH and pHRSRNFH4 were divided into one and three 
stages, respectively, according to their slopes changes and fitted with the 
following typical models (Wu et al., 2020): 
Zero-order model 
​ Qt = Q0 + k0(t − t0 ) (5) 
First-order model 
​ Qt = Q0 +
(
1 − e− k1(t− t0 )
)
(6) 
Higuchi model 
​ Qt = Q0 + kH(t − t0 )
0.5 (7) 
Where Q0 and t0 are constants to adjust the starting point of the release 
mechanism in response to changes in fertilizer hydrogel structure in the 
case where the initial fitting point is not the zero time in stages II or III. k 
is a kinetic constant that characterizes the release rate. Linear/nonlinear 
curve fitting using Origin software was applied to all the AN release 
profiles. The Korsmeyer-Peppas model equation is 
​ Qt = kK-Ptn (8) 
Where n is the release exponent. This model fits the entire release profile 
to illustrate a more detailed physical picture. 
2.7. Greenhouse pot trials with pHRSRNFH-based responsive/sustained 
AN delivery system 
To confirm the actual situation, the ability of the desired experi-
mental PHRSRNFH4 to release the AN steadily in response to the pH- 
stimulus of neutral soil/rice root under AWD irrigation in line with N 
plant demands during growth stages, water holding capacity, and 
biodegradability were tested. 
2.7.1. Experimental site and design 
The greenhouse pot experiment was conducted at the experimental 
agricultural farm (longitude 118◦83′E and latitude 31◦95′N) of the Soil 
and Water Engineering Department, Hohai University, Nanjing, China. 
The soil texture is clay loam with low total organic matter (27%) and is 
categorized as neutral soil (pH, 7.4). Thirty-three PVC pots were 
installed as an experimental group, and each pot (length: 80 cm, 
diameter: 16 cm) was filled with 10 kg of dry-grounded soil (see sup-
portive information). The experiment was laid out in a split-plot design 
with three replications. The main factor was the N-fertilizer delivery 
form, including three different N-fertilizer formulations as the following: 
positive control group treated with mineral AN-fertilizer (MF); group 
treated with control release AN-fertilizer hydrogel (CRNFH), and a 
group treated with the best formula of pH-responsive/sustained release 
AN-fertilizer hydrogels (pHRSRNFH4). The rate of N application in all the 
experimental pots under the different treatments corresponds to the N 
level of 175 mg.kg-1 soil (~138 kg N.ha− 1), which is the recommended 
level for rice production globally (Huang et al., 2018). In the MF group, 
1745 mg of free AN was injected into each pot at a depth of 10 cm below 
the soil surface to achieve the rate of 175 mg kg− 1 soil. Before planting, 
the dry granules of CRNFH and pHRSRNFH4 (containing 127.8 and 
172.5 mg N. granule− 1, respectively, with particles size ranging from 0.8 
to 10 mm) were buried in each experimental pot at a depth of 10 cm 
below the soil surface at a concentration of 0.14% and 0.10%, respec-
tively, to reach the N recommended level (Fig. 2S). AWD cycles are 
served by flooding soil with 5 cm water depth once the soil water con-
tent reaches 80-70% of saturation. A time-domain reflectometer moni-
tored soil water content. 
2.7.2. An release kinetic in the irrigated soil, plant, and N efficiency 
indicators with rice model 
To examine the AN release pattern from different N-fertilizer 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
6
formulations in the AWD-irrigated soil, 20 g of soil samples were 
collected at 10 days’ intervals through the wall holes of the tube in 
which sampling sippers were used to sample soil from the 0–40 cm layer 
of the root zone. Soil samples were air-dried, sieved, and bulked to make 
composite samples during the entire growing season, in addition to three 
months after harvest. Soil pH was measured in the composite samples 
during wetting/drying shifts in 1:5 soil-water extract using a calibrated 
pH meter. The contents of total N and mineral N forms (NH4–N +
NO3–N) in the composite samples resulting from AN release to the soil 
were determined by extraction with Morgan’s solution followed by 
determination of NH4–N/NO3–N by Nessler’s reagent, and phenol- 
sulphuric acid, respectively according to a standard method (Sahrawat 
and Prasad, 1975). 
To assess the efficiency of the experimental PHRSRNFH4 formulation, 
N nitration status, cell ultrastructure, and cell cycle progression in rice 
under different AN-fertilizer formulations application and AWD irriga-
tion in the neutral filed soil were evaluated. Therefore, FT-IR, trans-
mission electron microscopy (TEM), and flow cytometry analysis of rice 
leaves at the full panicle growth stage were carried out. Also, growth, 
yield, N crop removal (NCR), and NUE indicators of rice were observed 
(see supportive information for detailed methods). Root diameter (RD 
mm) and root weight density (RWD, g.cm − 3) is calculated as the 
following: 
RD =
̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅̅
RDW × 1
3.14 × RL
√
(9) 
RWD =
RDW
V
(10) 
Where RDW (g), RL (cm), and V (cm3) are the root dry weight, root 
length, and the soil core volume, respectively. 
The NCR (mg.plant− 1) was calculated by the following equations 
(Alhaj Hamoud et al., 2019): 
NCR= NAG + NAS =
(
NCG × DWG
100
)
+
(
NCS × DWS
100
)
(11) 
where NAG (g) and NAS (g) are the N accumulation in grain and straw. 
NCG (%) and NCS (%) are the N content in the grain and straw, 
respectively, measured according to (Jackson, 2005). (see supportive 
information) DWG (g) and DWS (g) are the dry weight of the grain and 
straw, respectively. 
The NUE was determined as the apparent N recovery efficiency 
(AREN, %), partial factor productivity (PFPN, g.g− 1), and the N harvest 
index (NHI, %) of N applied through different AN-fertilizer formulations 
by the following equations: 
AREN =
NCR
NI
× 100 (12) 
PFPN =
GY
NI
× 100 (13) 
NHI =
NAG
NAS + NAG
× 100 (14) 
Where NI (mg. soil− 1) is the nitrogen input, GY (g. plant− 1) is the grain 
yield. 
2.7.3. Biodegradation testing 
Masses of 10 g of fertilizer hydrogel granule samples were wrapped 
by 0.5 mm of polyethylene fine elastic-flexible net, and buried in 10 kg 
of field soil of the experimental greenhouse pot before planting at a 
depth of 10 cm below the soil surface. The amount of physical degra-
dation indicator at intervals of a month was monitored. The experiment 
was carried out in two alterations: samples of CRNFH and samples of 
pHRSRNFH4. For each alteration, further 12 independent biological 
replicates of the greenhouse pot experiment with a rice model were 
conducted. The fertilizer hydrogel granules in soil were regularly 
exhumed, washed free from soil, dried at 40 ◦C for 24 h, and weighed 
Fig. 2. (a) FTIR spectra and (b) zeta potential at varied pH of WS-substrates during the steps of ANA-CNF/PAM-PAEM hydrogels synthesis. 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
7
during the rice-growing season and after harvest to gauge the mass loss 
until the complete biodegradation (Boyandin et al., 2016). 
2.8. pHRSRNFH feasibility 
The economic evaluation of PHRSRNFH4 production was investigated 
regarding raw materials, operating costs, fixed capital investment (FCI) 
charges, general expenses of administration, and selling costs to deter-
mine the total production cost (TOC) per kilogram. The primary input 
data used in the TOC calculation are shown in Table 1S. 
2.9. Statistical analysis 
The IBM-SPSS statistical package version 19.0 was used to analyze 
the experimental data. The values of different variables were compared 
using the analysis of variance at (Pfree amine groups and the 
existence of electrostatic interactions or complexation in the different 
hydrogel formals during ANA-CNF/PAM-PAEM synthesis can also be 
confirmed and examined by zeta potential analysis. As shown in Fig. 2b, 
zeta potential values exhibited dependence on both pH, functionaliza-
tion, and activation with AN, which consequently will contribute to the 
pH-responsive swelling, AN release behavior, and the isoelectric point of 
the resultant hydrogel. Interestingly, the PAM functionalization with 
AEM increased the zeta potential of the resulting PAM-PAEM to +12.0- 
+31.4 mV in the acidic conditions, which corresponded to the related 
positive charge of AEM free amino group (NH3
+). Although the A-CNF 
incorporation into the hydrogel network rapidly further increases the 
related zeta potential of A-CNF/PAM-PAEM up to +43.2 mV due to free 
NH3
+ increase in the conjugates at the acidic conditions, AN embedding 
into ANA-CNF/PAM-PAEM slightly decreases zeta potential values close 
to +19.5-+39.8 mV again. This phenomenon agrees with FTIR finding 
that indicates the complex formation between AN anionic form with the 
hydrogel network, which may reduce the burst effect and result in sus-
tained AN release behavior of ANA-CNF/PAM-PAEM hydrogel. 
In practice, the higher positive charges of pHRSRNFH at the acidic 
media give the advantage of the greatest swelling, water uptake, and AN 
release in the lower soil pH during the wetting shifts applied in the 
neutral soil. In the meantime, the plant N requirements are maximal as 
the plant roots are activated by increasing water soil availability during 
wetting shifts. In the natural-to-alkaline media, the free NH3
+ is mostly 
protonated, and Zeta potential of ANA-CNF3/PAM-PAEM4 hydrogel de-
creases linearly, reaching the isoelectric point at pH ~7.4–7.8, which 
corresponds to the lowest swelling and AN release of the hydrogel. In 
practice, the isoelectric pH of ANA-CNF3/PAM-PAEM4 favorably 
matches the soil pH during drying shifts of the irrigation intervals 
(Fig. 4c), reducing N-volatilization/leaching loss when the N plant de-
mands are minimal as the roots are inactivated under low soil moisture 
content. 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
8
3.2. Surface morphology 
Morphological examination of the surface and pore structure was 
conducted using SEM images (Fig. 3) and BET analysis. The architectural 
structures of the swelled freeze-dried granule hydrogels embedded with 
AN-fertilizer were compared for differences due to their composition. 
The surface and cross-section of the ANPAM hydrogel (CRNFH) pre-
sented homogeneous and macroporous morphologies with the largest 
pores size and open-interconnected channels (Fig. 3a) that seemed to be 
the reason behind the relative highest/fastest AN release rate (Fig. 4). 
The solid crystalline structure of AN fertilizer was clearly highlighted in 
the structure of hydrogels, spotted and distributed homogeneously on 
Table 2 
The best-fitted parameters of the kinetic model for AN release from fertilizer hydrogels at various pH levels and incubation mediums. 
Media Hydrogel formulation Release stage Best-fitted Release parameters 
R2 K ( × 102, h− 1) 
pH 5.5 pH 7.4 pH 5.5 pH 7.4 
Buffer solutions pHRSRNFH4 I* First-order 0.997 0.997 0.068Aa 0.0599Ba 
II Zero-order 0.985 0.989 0.0027Aa 0.0025Ba 
III Higuchi 0.971 0.982 0.0281Aa 0.0276Ba 
VI Korsmeyer-Peppas 0.995 0.996 0.122Aa 0.114Ba 
CRNFH VI Zero-order 0.991 0.991 0.0071Aa 0.0071Aa 
VI Korsmeyer-Peppas 0.995 0.995 0.161Aa 0.161Aa 
Soil pHRSRNFH4 I First-order 0.997 0.999 0.060Ab 0.0575Bb 
II Zero-order 0.985 0.996 0.0025Ab 0.0023Ab 
III Higuchi 0.984 0.979 0.277Ab 0.0268Bb 
IV Korsmeyer-Peppas 0.996 0.995 0.115Ab 0.071Bb 
CRNFH VI Zero-order 0.968 0.968 0.0043Aa 0.0043Aa 
VI Korsmeyer-Peppas 0.994 0.994 0.126Aa 0.126 Ab 
*Stage I = 0–72 h, II = 144–504 h, III = 720–1660 h, and IV is the whole lifetime. Different uppercase letters within the same row and different lowercase within the 
same column indicate significant differences under different pH levels and media, respectively, at the same release stage (Plations was studied and modulated in the buffer solution and soil in the 
laboratory-test system at the targeted pH levels. As shown in Fig. 4 a-b 
and Table 2, the AN release studies indicated a dependence of AN release 
kinetics and its transport mechanisms on the hydrogels composition, the 
surrounding environment pH, and the release media itself. From Fig. 4 a- 
b, it was observed that the ANPAM hydrogel (CRNFH) copolymerization 
with up to 4 wt% AEM and 3 wt% A-CNFs, significantly improved their 
pH-sensitive properties and leading to much more sustained release 
behavior and slower release over time. The unique pH-sensitive profiles 
of ANA-CNF/PAM-PAEM (pHRSRNFH2-4) are attributed to the relative 
amino-functionalized surfaces, which introduced a special moiety elec-
trostatic repulsion/attraction status according to pH levels. Further-
more, the observed ionic interactions and hydrogen bonding between 
the AN anionic/cationic forms with the carbonyl, amine, and hydroxyl 
groups in pHRSRNFH2-4 networks (Fig. 2a) and their relative smaller 
pore sizes (Fig. 3b and c) effectively reduced their burst effect and AN 
diffusion rate (Table 2), improving sustained-release properties. 
As the pH range in the physiological conditions of neutral soils under 
AWD irrigation wetting/drying shifts is located at acidic/neutral-to- 
alkaline pH values, the pHRSRNFH2-4 was investigated within pH 5.5 
and pH 7.4 levels. The pHRSRNFH2-4 showed a significant pH-dependent 
AN release as a function of the targeted pH levels with the lowest and 
slowest rates in the neutral media while recording the fastest and highest 
rates in the acidic condition (Fig. 4 a-b). To explain this phenomenon, it 
has been previously indicated that the hydrogel swelling behavior is 
correlated with the isoelectric point and moieties repulsion, which 
subsequently govern the release of the loaded compound in this 
hydrogel material system. The ANA-CNF/PAM-PAEM hydrogel backbone 
contains ammonium moieties of –NH2 functional groups, which 
deprotonate and positively charge to NH3
+ in the acidic media, causing 
significant electrostatic repulsions (Fig. 2b), higher swelling, and 
eventually faster/higher AN release rate. With increasing the pH around 
the system, the amino groups gradually protonate, causing dramatically 
swelling decrease up to the net charge of the hydrogel becoming zero at 
the isoelectric pH of the corresponding hydrogel, pH 7–7.7 (Fig. 2a), 
resulting in the minimum AN release rates. 
Particularly, CRFNH exhibited the most rapid AN release rate (Kk-p =
0.161-0.126 × 102, h− 1) with a controlled release manner via Zeroth- 
order and no pH-responsive properties in an average of 19.4 and 14.5 
mg AN. Day− 1 from 1g of hydrogel for 9 and 12 days, in buffers and soil 
mediums, respectively, (Table 2). On the other hand, the pHRSRNFH4, as 
the best representative, showed typical pH-dependent/sustained AN 
release average of 3.00 and 2.69 mg.day− 1 at pH 5.5, while 0.92 and 
0.55 mg.day− 1at pH 7.4 from 1g of hydrogel for 58 and 65 days in 
buffers and soil, respectively (Fig. 4a and b, Table 2). 
In practice, the irrigated-neutral soil shows a dramatic pH decrease 
up to pH 4.9–5 after ~ 6–12 h of wetting shifts interval, followed by a 
dramatic pH increase during the drying shifts till reaching the initial soil 
pH value in the range of 6.5–7.5 (Fig. 5a). Herein, the lower soil pH 
environments under wetting shifts conditions combined with activated 
plant root acidity during these periods of irrigation intervals will 
favorably switch the faster/higher AN release rates from the pHRSRNFH4 
into the directly contacted soil and root surfaces in a sustained manner 
(Fig. 4c, Table 2). In contrast, the neutral soil pH during drying shifts 
(after 30–72 h application of irrigation intervals) will sufficiently reduce 
AN release rats from pHRSRNFH4 when the plant N requirements are 
minimal as the plant roots are inactive. These application properties of 
HRSRNFH4 will prevent N volatilization loss and improve N uptake and 
N use efficiency indicators (Table 3). 
As shown in Table 2, the whole lifetime of sustained AN release 
profiles of pHRSRNFH4 was divided into three release stages for the 
quantitative analysis of the AN release data according to their relative 
slopes changes and then best fitted with the suitable typical models. 
Under the different incubation media and pH levels, the PHRSRNFH4 
revealed the fastest AN release in the first stage with a short duration 
within 0–72 h incubation governed by the First-order mechanism (k1 =
0.068–0.0575). In this stage, A-CNFs in the PHRSRNFH4 begin to swell 
after incubation in buffer/soil mediums. Then, some of the uniformly 
distributed AN on the hydrogel network will diffuse, according to pH 
level, especially from the swollen regions of A-CNF surfaces into the 
inter-fiber spaces and the external medium. However, as the incubation 
time increases, the swelling continues. The diameter of A-CNFs increases 
until they fuse, leading to the denser matrix and fewer AN release 
channels and resulting in stage II release mechanism. From Table 2, it 
can be seen that, during stage II, the PHRSRNFH4 exhibited control 
release manners with the slowest AN release governed by the Zeroth- 
order mechanism with a longer duration (144–504 h). In this stage, 
the significant decreases in the AN release rate (k0 = 0.0023–0.0027) 
result in AN maintenance for a long time until the hydrogels begin to 
degrade. Finally, at the last release stages (720–1540 h), the hydrogel 
polymeric network was degraded after a long-time incubation, espe-
cially in the soil. Herein, A-NFCs mostly disappeared, the polymeric 
matrix broke up into oligomeric fragments, large pores were presented 
(Fig. 7b I-III), and the trapped AN in the dense hydrogel matrix was 
released by the Higuchi module with more rapid release rates again (kH 
= 0.0281–0.0268). Interestingly, the soil nature significantly slowed the 
AN release rate at all release stages and pH levels, leading to more stable 
AN release than buffer mediums. 
The starting point of each release stage related to a specific release 
mechanism was distinguished according to the relative slope changes of 
AN release data. These different three pH-dependent AN release stages 
are attributed to the changes in fertilizer hydrogel membrane structure 
as a function of the incubation time, A-NFC fibers swelling status, and 
hydrogel material degradation under different environmental condi-
tions changing found in the root zone as a result of irrigation, soil or-
ganism activity, and relative temperatures. 
Bringing AN release mechanisms/pH-responsive profiles of 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
11
pHRSRNFH4 and N plant requirements during different growth stages 
and conditions together, it is worth noting that pHRSRNFH4 offers 
optimal sustained AN doses delivery, covering N crop requirements 
during all the critical growth stages (e.g., from leafing to filling, Fig. 4c), 
compared to MF, and CRNFH that limited AN availability during the first 
growth stages only (Fig. 4a and b, and Fig. 5a). Another attractive point 
is that obtaining such a pH-responsive release profile of pHRSRNFH4 
favorably resulted in the highest/faster AN release at a lower pH soil 
environment after rewetting shifts, synchronizing with the maximum 
root activation periods at the higher water availability (Fig. 4a–c, and 
Fig. 5b), and improving root nutrients uptake. Conversely, the lowest/ 
slowest AN release at neutral pH mediums during drying shifts in the 
neutral soils reduces the AN loss; meanwhile, the roots are un-activated 
at low water availability. 
These unique pH-responsive properties and relativelysustained fer-
tilizer release mechanisms of pHRSRNFH4 are completely different from 
the situation where the fertilizer release is governed by control release 
mechanisms with no responsive properties in the elder CRNFH genera-
tion. Under the current study conditions, the related three sustained- 
release mechanisms of pHRSRNFH4 was founded to be comparable 
with that of CRNFH produced in this study which was followed the zero- 
order mechanism and released the total AN loaded after ~200–250 h 
incubation in buffers and soil, respectively, compared to 1600 h incu-
bation of pHRSRNFH4. Also, the release mechanisms and NA release time 
of pHRSRNFH4 are comparable with that resultes in several in-
vestigations on previous CRNFH generation based on cellulose and/or 
acrylamide hydrogels. For example, Poly (acrylic acid-co-acrylamide)/ 
cellulose nanofibrils nanocomposite hydrogels present urea desorption 
after about 192–240 h in a control release manner (Mahfoudhi and 
Boufi, 2016). Also, CRNFH based on bacterial cellulose-poly(acrylic 
acid-co-N, N′-methylene-bis-acrylamide) composite hydrogel exhibits 
nitrate ions desorption after about 80 h with no responsive behavior 
(Zaharia et al., 2018). The results were somehow expected because the 
addition of A-CNFs and AEM in the hydrogel composites not only led to 
denser polymeric networks and pH-responsive properties that resulted 
in a prolonged AN release from the pHRSRNFH4 but also the relative free 
amino group which resulted in interaction with the anionic part of AN 
together with the interaction between AN cationic form with the 
carbonyl group of PAM at pHRSRNFH4 backbone (Fig. 2), leading to less 
amount of AN on the hydrogel surface and retarding the release of AN 
over a longer period. While the poor interaction between the fertilizer 
and polymer, with no sensitive properties, and/or larger fiber size and 
pore size leads to a large amount of AN on the polymer surface that 
rabidly released in the elder CRNFH generation. 
3.4. AN release in the irrigated-neutral soil cultivated with rice under the 
greenhouse conditions 
The AN release in the irrigated-neutral soil was evaluated in three 
groups of greenhouse pots with rice (Fig. 2S) that were separately 
treated by different AN-fertilizer formulations of PHRSRNFH4, CRNFH, 
and MF. As shown in Fig. 5a and b, the main factors determining the AN 
release in the irrigated soil were the AN-fertilizer formulation, time after 
application, and soil pH fluctuations related to the soil water content 
changes during wetting/drying shifts of AWD irrigation (Fig. 5b). As 
Fig. 5. (a) The total N and mineral N contents in the irrigated-neutral soil resulting from AN release of different AN-fertilizer formulations under the greenhouse-test 
system with rice. (b) The total N content resulting from AN release of different 25 days AN-fertilizer formulations as a function of soil pH related to time after ADW 
irrigation intervals application. 
Table 3 
Development of the rice/N efficiency indicators as a function of the application 
of different AN-fertilizer formulations under AWD irrigation of the neutral field 
soil. 
Indicator AN fertilizer hydrogel formulation 
PHRSRNFH4 CRNFH MF 
Growth RD (mm) 0.57 ± 0.02a 0.47 ±
0.04b 
0.39 ±
0.02c 
RWD (g.cm− 3) 0.52 ± 0.04a 0.30 ±
0.01b 
0.21 ±
0.02c 
Number of tillers (tiller. 
plant− 1) 
43.0 ± 4.07a 33.7 ±
1.2b 
27.7 ±
1.7c 
Yield Panicles’ number 
(panicle.plant− 1) 
41.3 ± 4.6a 25.7 ±
1.9b 
21.0 ±
1.4b 
Total biomass (g. 
plant− 1) 
60.6 ± 1.8a 47.0 ±
2.7b 
33.4 ±
1.6c 
Grain yield (g.plant− 1) 29.6 ± 2.6a 21.6 ±
1.7b 
15.9 ±
1.6c 
NCR NAG (mg.plant− 1) 579.5 ±
17.5a 
357.8 ±
21.5b 
169.5 ±
11.8c 
NAS (mg.plant− 1) 215.4 ±
21.8a 
170.4 ±
15.6b 
94.4 ±
12.8c 
NUE AREN (%) 57.8 ± 1.7a 38.4 ±
1.4b 
19.2 ±
0.4c 
PFPN (g.g− 1) 21.5 ± 0.6a 15.7 ±
0.9b 
11.5 ±
0.3c 
NHI (%) 74.9 ± 2.6a 67.6 ±
5.8b 
64.3 ±
4.6b 
Note: Different uppercase letters within the same raw indicate significant 
differences (PN nutrition when 
rice plant root is activated. 
Further investigation at the cell ultrastructure level of rice leaves was 
explored by TEM analysis (Fig. 6b). Under MF treatments, the TEM 
analysis showed thick cell wall (CW), a lot of the vacuoles (Va), raptured 
chloroplasts (Chl), small thylakoids (Thy), and abnormal starch grains 
(SG), indicating induced cell development as a result of the poor N 
nutrition status. Conversely, the optimal N nutrition status under 
pHRSRNFH4 treatment considerably improved the cell ultrastructure of 
the typical cell walls, developed chloroplasts, uniform-large thylakoids, 
typical starch grains, and vacuoles absence was observed. Also, the 
nuclear DNA contents by flow cytometry for rice leaves were assayed to 
investigate whether the various fertilizer formulations affect the cell 
cycle progression during a specific cell cycle phase. As shown in Fig. 6c, 
the results demonstrated that each treatment affects the cell cycle 
development in a different range manner. Unsurprisingly, the optimal N 
nutrition status resulting under pHRSRNFH4 treatment greatly encour-
aged the progress of plant cells through the cell cycle compared to the 
changes in cell progression induced by CRNFH and MF treatments. 
In agreement with the development in N nutrition status and cell 
progression after serving PHRSRNFH4, the growth, yield, crop N 
removal, and NUE indicators showed significant enhancement 
compared to their values after CRNFH free AN application (Table 3). In 
particular, under PHRSRNFH4, the RWD and RD considerably boosted 
compared to that under CRNFH and MF treatments, producing superior 
rice root growth in contact with the soil and the dense penetration into 
fertilizer hydrogel themselves (Fig. 7bIV, Fig. S2). The vigorous roots 
were due to N availability within the rhizosphere during the root activity 
periods and the rice’s different growth stages (Figs. 4 c, Fig. 5 a-b), 
which consequently improved N plant uptake (Alhaj Hamoud et al., 
2019). These results can coordinate with the largest shoot biomass, 
producing 43 tiller/plant, contributing to the best N uptake, overall 
plant growth, and thus rice productivity (Table 3). The maximum N 
concentration in the root zone throughout the growing season (Fig. 5a) 
and the superior plant root/shoot activity eventually led to the largest 
responsiveness to N. Subsequently, an abundant amount of N ions were 
fixed in plant particles which corresponded to the maximum NCR values 
under PHRSRNFH4 treatments. As the PHRSRNFH4 application maxi-
mally increased N availability, rice root/biomass activities and their 
utilization efficiency regarding N uptake thus, resulted in the most sig-
nificant N accumulation in larger biomass and the highest values of 
ANRE, PFPN, and NHI. 
Furthermore, the ideal AN supply in a sustained/pH-responsive 
manner reduced the N loss by volatilizing/leaching and increased the 
N recovery by 19.4% and 38.6% compared to the AN supply via control 
release manner using CRNFH and free AN treatment, respectively. 
Equally, the worse N nutrient regime created by MF sharply increased N 
loss and decreased N availability, especially after 30 days’ application. 
This reduced the utilization of AN applied and subsequently N accu-
mulation in the plant, resulting in the lowest NUE of N applied (Table 3). 
3.6. The biodegradability and feasibility evaluation of PHRSRNFH4 
As shown in Fig. 7a, the initial mass loss began in the first month in 
the PHRSRNFH4, followed by steady degradation ending with approxi-
mately 52% of its original mass at harvest until the complete degrada-
tion at 10th month after incubation. Despite being subjected to a large 
amount of water exposure of irrigation and to plant root activity during 
the growing season, CRNFH was able to avoid initial mass loss about the 
first 3 months, and only 23% of their original mass was observed at 
harvest until the complete degradation at 16th month after incubation. 
The faster degradation was attributed to A-CNFs biocompatibility and 
the hydrophilic aggregation of amino groups at the PHRSRNFH4 
network, which increased its hydrophilicity, water uptake, and water- 
holding capacities (Fig. 3d, f) (Park et al., 2003). Thus, promoting a 
dense root-penetration feature (Fig. 7bIV), soil degradation organisms 
attach to its polymeric matrix, further accelerating its physical/chemical 
biodegradation rate (Chamas et al., 2020; Xiong et al., 2018). Interest-
ingly, the presence of AN crystals at the 3rd month of PHRSRNFH4 
application (Fig. 7bIII) explained the stage III of sustained AN release 
that was governed by Higuchi module (720–1660 h) (Fig. 4) resulted by 
hydrogel biodegradation. 
To evaluate production facilities and highlight the advantage of 
PHRSRNFH4 over the elder generation of superabsorbent hydrogels 
(SAH) and CRFH, a preliminary economic evaluation to estimate the 
TPC of PHRSRNFH4 was established. The TPC was calculated based on 
manufacturing costs, which include the raw materials costs estimated 
according to actual consumption from experimental results, and 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
13
Fig. 6. (a) Deconvolution Curve-fitting, (b) TEM micrographs, and (c) ungated histogram and a scatterplot of flow cytometry analysis of cell cycle with leaf bio-
masses graphs under different AN fertilization formulations at the full panicle growth stage. 
H. Shaghaleh et al. 
Journal of Cleaner Production 368 (2022) 133098
14
operating costs which contain A-NFC production costs mainly, and other 
components related to FCI charges (Table 1S), in addition to general 
expenses of administration and selling costs. According to the input 
parameters for calculations presented in Table 1S for TPC estimation, 
the raw materials with A-NFC production cost were 1.28 USD.kg− 1, and 
the TPC of PHRSRNFH4 was about 2.59 USD.kg− 1, which is comparable 
to SAH and CRFH costs. For example, according to Alibaba international 
prices, the polymer-coated urea and SAH-based polyacrylate hydrogels 
cost about 0.88–1.51, and 3.55–4.25 USD.kg-1, respectively significant 
potential of PHRSRNFH4 to serve as an alternative fertilizer formulation. 
4. Conclusions 
In this study, AN-loaded A-CNF/PAM-PAEM hydrogel for developing 
a pH-responsive/sustained release N-fertilizer delivery system in 
response to pH triggers fluctuation of the neutral soils during wetting/ 
drying shifts of irrigation and different growing season stages was suc-
cessfully synthesized. The AEM and A-CNF addition leads to desirable 
enhancement of surface characterization, water uptake, fertilizer 
loading efficiency, pH-responsive/sustained release behavior, and 
biodegradability of as-prepared fertilizer hydrogels. The selectively 
functionalized PHRSRNFH4 exhibits the preferred slowest/lowest AN 
release at a neutral pH medium compared to the most active AN release 
rates at the lower pH conditions with sustained AN supplying over 90- 
days the neutral-irrigated soil cultivated with rice. Such fertilizer de-
livery pattern leads to desired N-fertilizer management being synchro-
nized with plant demands along with the critical growth periods and 
root activation under short-term pH changes of neutral soils during 
wetting/drying of irrigation intervals. Consequently, applying this new 
pH-responsive/sustained AN delivery system considerably improved 
plant/N use efficiency indicators by offering optimal N application rate 
with suitable water holding capacity and biodegradation rate