Next Article in Journal
Nano-Agrochemicals as Substitutes for Pesticides: Prospects and Risks
Next Article in Special Issue
Quantifying the Individual and Combined Effects of Short-Term Heat Stress at Booting and Flowering Stages on Nonstructural Carbohydrates Remobilization in Rice
Previous Article in Journal
Trends in the Tissue Culture Techniques and the Synthesis of Bioactive Compounds in Eurycoma longifolia Jack—Current Status and Future Perspectives
Previous Article in Special Issue
Calcium-Dependent Protein Kinase 5 (OsCPK5) Overexpression in Upland Rice (Oryza sativa L.) under Water Deficit
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 13
Issue 1
10.3390/plants13010108
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effects of Waterlogging at Flowering Stage on the Grain Yield and Starch Quality of Waxy Maize

by
Huan Yang
,
Xuemei Cai
and
Dalei Lu
*
Jiangsu Key Laboratory of Crop Genetics and Physiology, Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou 225009, China
*
Author to whom correspondence should be addressed.
Plants 2024, 13(1), 108; https://doi.org/10.3390/plants13010108
Submission received: 6 November 2023 / Revised: 24 December 2023 / Accepted: 27 December 2023 / Published: 29 December 2023
(This article belongs to the Special Issue Abiotic Stresses in Cereals)
Browse Figures
Review Reports Versions Notes

Abstract

:
Waterlogging is a common abiotic stress in global maize production. Maize flowering stage (from tasseling to silking) is more fragile to environmental stresses, and this stage frequently overlapped the plum rain season in the middle and lower reaches of Yangtze river in China and affect the yield and quality of spring-sown maize severely. In the present study, the soil moisture content under control and waterlogging conditions at the flowering stage was controlled by a negative-pressure water supply and controlling pot device in a pot trial in 2014–2015. The grain yield, starch content, and starch structural and functional properties under two soil moisture levels were compared using Suyunuo5 (SYN5) and Yunuo7 (YN7) as materials, which are the control hybrids of National waxy maize hybrid regional trials in Southern China. The results observed that the grain yield was reduced by 29.1% for SYN5 with waterlogging due to the decreased grain weight and numbers, which was significantly higher than that of YN7 (14.7%), indicated that YN7 was more tolerant to waterlogging. The grain starch content in YN7 was decreased by 9.4% when plants suffered waterlogging at the flowering stage, whereas the content in SYN5 was only decreased in 2014 and unaffected in 2015. The size of starch granules and proportion of small-molecule amylopectin with waterlogging at the flowering stage increased in SYN5 and decreased in YN7 in both years. The type of starch crystalline structure was not changed by waterlogging, whereas the relative crystallinity was reduced in SYN5 and increased in YN7. The pasting viscosities were decreased, and the pasting temperature was unaffected by waterlogging in general. The gelatinization enthalpy was unaffected by waterlogging in both hybrids in both years, whereas the retrogradation enthalpy and percentage in both hybrids were reduced by waterlogging in 2014 and unaffected in 2015. Between the two hybrids, YN7 has high pasting viscosities and low retrogradation percentage than SYN5, indicated its advantages on produce starch for more viscous and less retrograde food. In conclusion, waterlogging at the flowering stage reduced the grain yield, restricted starch accumulation, and deteriorated the pasting viscosity of waxy maize. Results provide information for utilization of waxy maize grain in food production.

1. Introduction

In the current climate change scenario, agriculture faces increasing instability with extreme weather events, leading to considerable yield losses [1]. Waterlogging is a prevalent environmental adversity that suppresses maize (Zea mays. L) productivity and degrades grain quality; it is predicted to increase in magnitude and frequency along with global warming [2]. In South and Southeast Asia alone, 18% of the total maize growing area is frequently affected by waterlogging, which dominates 25–30% of annual production losses [3]. Maize is a rainfed crop and is considered vulnerable to waterlogging when the field soil moisture content is higher than 80%, thereby affecting plant growth and development [4]. Among different growth stages, ranking of the daily water requirement of maize from high to low was the flowering to the silking stage, the tasseling to the flowering stage, the jointing to the tasseling stage, the silking to the harvesting stage, and the lowest at the sowing to the emergence stage [5]. Among different stages of maize, waterlogging occurred at the jointing stage had the greatest effect on maize growth and grain yield, followed by seedling, tasseling, and milk maturity stages, and the 100-grain weight and grains per ear had the largest effect on grain yield, and the severity gradually increased with the lengthening of waterlogging duration [6]. In comparison, another study reported that 6-day waterlogging at the seedling stage was more severe than occurred at the jointing and tasseling stages [7,8]. In the middle and lower reaches of the Yangtze river, plum rain season usually prevails in June, which overlapped with the spring-sown maize late growth stages, and severely affects plant pollination and grain filling, and ultimately results in yield loss. Waterlogging around the flowering stage induces the increase in lodging risk by decreasing the stem diameter, rind penetration strength, and transverse bending strength of the third base internode [4]. Waterlogging also decreases the chlorophyll and carbohydrate contents [9] and the nitrogen content in different organs at silking and maturity stages [10]. Waterlogging also disturbs carbon-nitrogen metabolism, breaks plant endogenous hormone balance, accelerates leaf senescence, eventually results in a significant reduction in photosynthetic capacity and maize grain yield [11,12,13].
Starch is the dominant storage substance (~70%) of the grains, and it determines the grain quality. Among different processing qualities, pasting and thermal properties are the two most important indexes; pasting properties reflect the starch viscosity during the heating and cooling stages; thermal properties, including gelatinization and retrogradation, which reflect the thermal stability and are determined by starch structural parameters such as granule size, amylopectin chain length, molecular weight distribution, etc. Both pasting and thermal properties can provide information for starch production and utilization [14]. Waterlogging affects grain starch formation, deposition, and structural and functional properties. Waterlogging starting at the anthesis stage decreases the amyloplast number in the wheat endosperm and advances the programmed cell death in endosperm cells [15]. Post-anthesis waterlogging suppresses the activities of ADP glucose pyrophosphorylase and soluble starch synthase in wheat grains, increases the starch granule size, and reduces the viscosity parameters [16,17]. Meanwhile, waterlogging during grain filling decreases the grain weight and affects the milling quality, although changes in protein composition may increase or maintain the gluten strength [18]. However, the short duration of waterlogging and shading decreases the size of starch granules and increases the peak viscosity (PV) [19]. In rice, the structural and pasting characteristics of starch are affected by flooding irrigation, but the influence varies among cultivars [20]. In comparison with alternate wetting and drying, constant-flooding irrigation decreases the PV, breakdown (BD), and setback (SB) viscosities, gelatinization enthalpy (ΔHgel), and temperatures; however, the effect on starch granule size and amylopectin chain length distribution has different trends [21]. In peanuts, the contents of oil, unsaturated fatty acids, and starch in grain increased, while the contents of crude protein, soluble sugar, saturated fatty acids, and amino acids (essential, non-essential, and total) decreased under waterlogging [22]. Waxy maize is a special maize type with starch is composed of nearly pure amylopectin, which endows its high viscosity, low retrograde, and high stability than normal maize starch and widely used in some industries such as thickening agent, emulgator, adhesive, suspending agent, etc. [23]. Suyunuo5 (SYN5) and Yunuo7 (YN7) are two widely planted hybrids in Southern China, and both hybrids are the controls of the National waxy maize regional trials [24]. Our previous studies reported that waterlogging during the grain filling stage has significantly affected the starch physicochemical properties [25,26]. However, limited information is available regarding the starch deposition and functional properties of waxy maize that suffered waterlogging at the flowering stage. We hypothesize that waterlogging at the flowering stage affects starch accumulation and changes the starch structure, thereby affecting the starch physicochemical properties, such as the pasting and thermal properties of waxy maize. Results could provide a fundamental basis for using stressed starch based on the utilization of waxy maize.

2. Results and Discussion

2.1. Grain Yield

The grain weight was significantly reduced by waterlogging in both hybrids in both years, with a decrease of 8.4% and 23.5% for YN7 and SYN5, respectively (Figure 1). The grain number was also reduced by waterlogging in both hybrids in both years (6.7% for YN7 and 7.5% for SYN5), and the decrease was significant for SYN5 in 2015 and for YN7 in 2014. The reduced grain weight and number induced the yield loss in both years, and the decrease was 14.7% for YN7 and 29.1% for SYN5, indicating that YN7 was more tolerant to waterlogging at the flowering stage than that of SYN5. Yield penalty due to waterlogging at the flowering stage has been widely reported in maize and is mainly related to the decreased grain number and weight. These yield penalties may relate to the decreases in post-silking dry matter accumulation, redistribution of stored photosynthate to the grain, and the conversion capacity from carbohydrate to starch in grain [27]. This observation was caused by decreased activities of ribulose bisphosphate carboxylase and phosphoenolpyruvate carboxylase, decreased the contents of zeatin riboside, indole-3-acetic acid, and gibberellic acid but increased abscisic acid in leaf, and reduced photosynthetic rate by disordered the leaf gas exchange parameters and chlorophyll fluorescence parameters [11,12,13], which resulted in the decreased antioxidative enzyme activities, accelerating leaf senescence, and ultimately leading to the decreased biomass accumulation [27]. The yield for YN7 under different treatments was higher than that for SYN5 due to it having more grain numbers and higher grain weight, which is similar to our previous study [28]. Between two years, the grain yield was lower in 2014, which may be due to this year suffering high temperatures and low sunlight during grain filling stages.

2.2. Starch Content

The starch content in YN7 was significantly decreased by waterlogging (6.3% and 12.5% in 2014 and 2015) in both years; the value in SYN5 was unaffected in 2015 and decreased by 6.7% in 2014 (Figure 1). The unaffected starch content in SYN5 in 2015 may be due to the severe yield decrease this year, and the shrunken sink makes the surviving grains receive a similar source. Our previous study on fresh waxy maize (harvested at the milk stage) observed that the starch content was increased due to the accelerated grain filling and shortened grain filling duration [28], as the starch content increased gradually with grain filling proceeding, but the shortened filling duration results in lower starch content in the grain that harvested at maturity. Zhou et al. [17] observed that post-anthesis waterlogging reduced the wheat grain amylose content but did not affect the amylopectin content. The reduced starch content may be caused by the weakened activities of sucrose synthase and soluble starch synthase [27] and decreased the allocation of nitrogen and carbon assimilates at pre- and post-anthesis to the grains [29]. A study on peanuts also reported that the decreased starch content under waterlogging at the flowering stage was mainly caused by the decreased activities of sucrose synthetase and sucrose phosphate synthetase [30].

2.3. Starch Granule Size

The size distributions of starch granules under different treatments presented dual peaks (Figure 2). The average starch granule size in response to waterlogging differed between the two hybrids; the size increased in SYN5 but decreased in YN7 in both years when the plants suffered from waterlogging at the flowering stage (Table S2). A study on rice also observed that the starch granule size in response to constant flooding irrigation management differed between the two cultivars [21]. Waterlogging during heading and anthesis stages causes damage to wheat endosperm cell structure, decrease the starch granules numbers in endosperms, result in the formation of irregular starch granules and enlarge the starch granule size [17]. Another study reported that short-time waterlogging and shading decreased the starch granules size [19]. Our previous study reported that the starch granule size of the two hybrids was decreased by post-silking waterlogging [25]. In the present study, the discrepancy in the results between the two hybrids may be due to the different features of their development; the amyloplast in the endosperm in SYN5 was formed late and less but developed quickly, whereas the starch granules in YN7 formed more number in endosperm cells [31]. Therefore, amyloplast formation in endosperm cells needs further study to clarify the discrepancy in different hybrids.

2.4. Starch Molecular Weight Distribution

The molecular weight distribution of isoamylase debranched starch for all the samples presented dual peaks, namely, peak 1 and peak 2 (Figure 3), consistent with those of different waxy starch resources, indicating its typical waxy starch character [32]. In the GPC profiles of amylopectin, the peak 1 fraction contains short starch chains, such as A and B chains (A + B1 chains), and the peak 2 fraction consists of long B chains with high-molecular-weight molecules [33]. The peak 1/peak 2 value with waterlogging significantly increased in SYN5 but decreased in YN7 in both hybrids, consistent with the change trends of starch granule size; this finding indicated that starch with large granule size has a high proportion of small molecular size of amylopectin branch chains [32]. A study on rice observed that the amylopectin chain length in response to constant-flooding irrigation management differed between the two cultivars [21].

2.5. Starch X-ray Diffraction

The X-ray diffraction (XRD) of starch provided information on the long-range molecular order and was associated with ordered arrays of double helices formed by the amylopectin side chains [34]. All the samples presented refection angles at 15°, 23°, 17°, and 18°, which present typical “A” diffraction pattern (Figure 4). The relative crystallinity (RC) with waterlogging significantly decreased in SYN5 but increased in YN7 in both years. The different responses of RC to flooding irrigation were also reported in rice [20]. In the present study, the change trend of RC was contrary to the trend of starch granule size and peak 1/peak 2 ratio, indicating the starch with large granule size and high molecular weight has low RC. Our previous study also observed that waxy maize starch with a high proportion of medium-sized starch granules has high RC [35]. Hsieh et al. [32] reported that waxy starch with a small granule size and a high proportion of peak 1 has high RC.

2.6. Pasting Property

The grain flour PV, SB, trough (TV), and final (FV) viscosities in SYN5 were reduced by waterlogging in both years, whereas the BD was reduced and unaffected by waterlogging in 2014 and 2015 (Table 1). The pasting viscosities of YN7 were decreased by waterlogging in 2014. The PV and BD were reduced, whereas the TV, FV, and SB were unaffected in 2015. The pasting temperature (Ptemp) in YN7 was unaffected by waterlogging in both years, whereas the value in SYN5 was unaffected in 2014 but decreased by waterlogging in 2015. In general, the pasting viscosities were decreased, and Ptemp was unaffected by waterlogging. The decreased viscosities indicated the waterlogged waxy maize starch was less broken during heating, and the cracked granule was less re-associated after cooling to room temperatures. This finding is consistent with the observation on wheat [16,17] and our previous study on waxy maize starch [25,26]. The decreased viscosity is mainly due to the decreased starch content [36]. However, a study on wheat observed that short-time (7 d) waterlogging and shading increased the PV and Ptemp but decreased the TV and FV [19]. In rice, the pasting viscosity in response to waterlogging differed among the cultivars [20]. YN7 has higher PV, BD, FV, and SB than SYN5, but they have similar TV and Ptemp. This finding indicated that YN7 has an advantage in producing viscous foods.

2.7. Thermal Property

The gelatinization and retrogradation characteristics of waxy maize flours under different water conditions are presented in Table 2. The ΔHgel was unaffected by waterlogging in both hybrids in both years, whereas the ΔHgel in response to post-silking waterlogging was dependent on hybrids [26]. A study on rice also observed that ΔHgel with constant flooding irrigation was higher than that of alternate wetting and drying irrigation, but it, compared with conventional irrigation, fluctuated between cultivar and year [21]. The To and Tp in SYN5 were reduced by waterlogging in both years; the two parameters in YN7 were reduced and unaffected by waterlogging in 2014 and 2015, respectively. The Tc in SYN5 was unaffected and decreased by waterlogging in 2014 and 2015, respectively. The Tc in YN7 was unaffected and increased by waterlogging in 2015 and 2014, respectively. Constant-flooding irrigation reduced the transition temperature of starch in rice [21], indicating that waterlogging reduced the stability of the starch structure [23].
Retrogradation occurred after the gelatinized samples were stored at 4 °C for 7 days. The ΔHret and %R in both hybrids were decreased by waterlogging in 2014 and were unaffected in 2015. Our previous study observed that the %R was increased by waterlogging after pollination [26]. The discrepancy may be due to the plants grown in 2015 having longer rainfall duration during grain filling (211 and 445 mm in 2014 and 2015, respectively); the adequate rainfall erased the influence of waterlogging during flowering. Between the two years, the thermal characteristics of plant growth in 2015 were significantly higher than that in 2014. The two hybrids have similar ΔHgel and To, but SYN5 has higher Tp, Tc, ΔHret, and %R than YN7, which endows the advantage of YN7 to produce low retrograde food.

3. Materials and Methods

3.1. Experimental Design

A pot trial was conducted on the Experimental Farm at the Agricultural College of Yangzhou University, China, in 2014–2015. Two control hybrids (SYN5 and YN7) of the National waxy maize regional trial were selected as the plant materials as those two hybrids were widely planted in Southern China. Seeds were sown on March 15 in both years. The two seedlings at the one-leaf stage were transplanted to pots (38 cm height and 43 cm diameter), and one seedling at the jointing stage was left. Each treatment included 30 pots. The soil organic matter, total N, mineral N, test P, and test K contents were 19.5 g/kg, 1.23 g/kg, 69.1 mg/kg, 35.7 mg/kg, and 86.2 mg/kg in 2014, and were 17.3 g/kg, 1.21 g/kg, 100.2 mg/kg, 33.6 mg/kg, and 124.5 mg/kg, respectively. The plants were supplied with 10 g of compound fertilizer (N:P2O5:K2O = 15%:15%:15%) at transplanting time and 6 g of urea (N = 46%) at the jointing stage [25]. The weeds in the pot were manually removed. The mean temperature, rainfall, and sunlight durations during plant growth in 2014 and 2015 were 21.73 and 21.00 °C, 426 and 730 mm, and 599 and 500 h, respectively (Table S1).
Soil moisture content was controlled by a negative-pressure water supply and controlling pot device [37] by setting the water supply tension of the device at different values [24]. Before the tasseling, the soil’s relative moisture content was set at 75%. At the flowering stage (from tasseling to silking), the soil relative moisture content for control (CK) and waterlogging (WS) was set at 80% (75~85%) and over 100% (10 mm water level aboveground). Stress was terminated after the ears were manually pollinated. During treatment, the plants were covered with a transparent canopy that was 5 m high aboveground to avoid the influence of rainfall. After treatment, the soil’s relative moisture content was reset to approximately 75% until maturity.

3.2. Grain Yield

The grains were harvested at maturity (about 40 days after pollination), and the grain number per ear was counted. The grains were manually stripped from the cobs, and grain weight (mg) and grain yield (g/plant) were determined after sun drying.

3.3. Starch Content

Starch content in grains was determined with anthrone–sulfuric acid method [38].

3.4. Starch Isolation

The grains were steeped in 1 g/L NaHSO3 solution at room temperature for 2 days. The starches were isolated using the method described by Lu et al. [24]. The samples were rinsed with distilled water and then ground using a blender for 2.5 min. The suspensions were passed through a 100-mesh sieve. The residues on the screen were again homogenized for 1.5 min and then passed through the same sieve. The starch–protein slurry was collected in a 1000 mL wide-neck flask and allowed to stand for 4 h. The supernatant was suctioned, and the settled starch layer was collected in 50 mL centrifuge tubes and centrifuged at 3000× g for 10 min. The upper non-white layer was scooped. The white layer was resuspended in distilled water and stirred for 30 min before centrifugation. The isolation procedures were repeated thrice. The starch was then collected and dried in an oven at 40 °C for 48 h. The protein and ash contents in the isolated starch were determined by using the International Methods 46-10.01 and 08-17.01 of AACC. These contents were lower than 0.3% and 0.2%, indicating that the purity of starch was up to the Chinese National Standard (GB/T 8885-2017) [39].

3.5. Starch Granule Size

The average starch granule size (µm) was expressed in terms of the volume of equivalent spheres. The size distributions of starch granules were estimated with a laser diffraction particle size analyzer (Mastersizer2000, Malvern, Worcestershire, UK) following a procedure described in the study of Lu et al. [24]. The disperse phase was absolute ethyl alcohol. Instrument accuracy was verified by using Malvern standard glass particles. The instrument, which follows the principle of laser diffraction, can measure sizes of 0.1 and 2000 μm.

3.6. Starch Molecular Weight

For isoamylase debranched starch granules, starch (5 mg) was dissolved in 5 mL of distilled deionized water in a boiling water bath for 60 min. Sodium azide solution (10 µL 2% w/v), acetate buffer (50 µL, 0.6 M, pH 4.4), and isoamylase (10 µL, 1400 U, EC 3.2.1.68, Sigma, Sigma Chemical Co., St. Louis, MO, USA) were added to the starch dispersion. The mixture was incubated in a water bath at 37 °C for 24 h. The hydroxyl groups of the debranched glucans were reduced by treatment with 0.5% (w/v) of sodium borohydride under alkaline conditions for 20 h. The preparation of about 600 µL was dried in vacuo at room temperature and allowed to dissolve in 20 µL of 1 M NaOH for 60 min. The solution was diluted with 580 µL of distilled water.
Molecular weight distribution was analyzed using a PL–GPC 220 high-temperature chromatograph (Agilent Technologies UK Limited; Shropshire, UK) with three columns (PL110–6100, 6300, and 6525) and a differential refractive index detector [40,41]. The eluent system used dimethyl sulfoxide containing 0.5 mM NaNO3 at a flow rate of 0.8 mL/min. The temperature of the column oven was controlled at 80 °C.

3.7. X-ray Diffraction

X-ray diffraction patterns of starch were obtained with an X-ray diffractometer (D8 Advance, Bruker–AXS, Karlsruhe, Germany) operated at 200 mA and 40 kV. The scanning region of diffraction angle (2θ) ranged from 3° to 40° at a step size of 0.04° with a count time of 0.6 s. Relative crystallinity (RC, %) was calculated as the percentage of the sum of total crystalline peak areas to total diffractograms.

3.8. Pasting Property

The pasting properties of starch (1.96 g of starch added in 26.04 g of water, total weight of 28 g; 7% db, w/w) were estimated using a rapid viscosity analyzer (RVA, Model 3D; Newport Scientific, Warriewood, NSW, Australia) following the method of Lu et al. [26]. A sample suspension was equilibrated at 50 °C for 1 min, heated to 95 °C at 12 °C/min, maintained at 95 °C for 2.5 min, cooled to 50 °C at 12 °C/min, and maintained at 50 °C for 1 min. The paddle speed was set at 960 rpm for the first 10 s and then decreased to 160 rpm for the rest of the analysis.

3.9. Thermal Property

The gelatinization properties of starch were estimated by differential scanning calorimetry (DSC, Model 200 F3 Maia, NETZSCH, Waldkraiburg, Germany) following the method of Lu et al. [26]. Each sample (5 mg, dry weight) was loaded into an aluminum pan (25/40 microliters, D = 5 mm), and distilled water was added to achieve a starch-water suspension containing 66.7% water. Samples were hermetically sealed and allowed to stand for 24 h at 4 °C before heating in the DSC. The DSC analyzer was calibrated using an empty aluminum pan as a reference. Sample pans were heated at a rate of 10 °C/min from 20 to 100 °C. Thermal transitions of starch were defined as onset temperature (To), peak gelatinization temperature (Tp), conclusion temperature (Tc), and gelatinization enthalpy (ΔHgel). Samples were stored at 4 °C for 7 days after thermal analysis for retrogradation investigations. Retrogradation enthalpy (ΔHret) was automatically calculated, and retrogradation percentage (%R) was computed as %R = 100 × ΔHret/ΔHgel.

3.10. Statistical Design

Data presented in tables and figures are the mean of three repetitions (ten plants compose a repeat). Analysis was performed using ANOVA and Duncan’s test at a significance level of p < 0.05 with the data processing system (version 7.05).

4. Conclusions

Waterlogging stress at the flowering stage decreased the grain number and weight, resulting in yield loss. The grain starch content was reduced by waterlogging. The size of starch granules was enlarged and reduced by waterlogging in SYN5 and YN7, respectively. The proportion of high-molecular weight in amylopectin and RC were decreased and increased by waterlogging in SYN5 and YN7. The grain flour pasting viscosities were reduced by waterlogging in general. The ΔHgel was unaffected, and the transition temperatures were reduced by waterlogging in general. The ΔHret and %R in both hybrids were reduced and unaffected by waterlogging in 2014 and 2015, respectively. YN7 had higher pasting viscosity and lower %R than SYN5 and is superior in producing food with a more viscous taste and low retrograde. In addition, YN7 was more tolerant to waterlogging, indicating this hybrid has an advantage in growing in stressful conditions. The plants’ growth in 2015 with adequate rainfall during grain filling achieved higher grain yield, PV, BD, and %R. The results offer the option to choose an optimal waxy maize hybrid under normal and waterlogged conditions based on different food utilizations.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants13010108/s1, Table S1: Meteorological conditions during plant growth in 2014 and 2015, Table S2: Effects of waterlogging at the flowering stage on the flour pasting property of waxy maize.

Author Contributions

H.Y.: Investigation, Formal analysis, Writing—Original draft, Writing—Review and editing. X.C.: Investigation, Formal analysis. D.L.: Conceptualization, Funding acquisition, Methodology, Supervision, Validation, Writing—Review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the earmarked funds for Jiangsu Agricultural Industry Technology System (JATS[2022]497, JAT[2023]S454), Key Research and Development Program of Jiangsu Province (BE2021317), Priority Academic Program Development of Jiangsu Higher Education Institutions, and High–end Talent Support Program of Yangzhou University.

Data Availability Statement

All the data and code used in this study can be requested by email to the corresponding author Dalei Lu at dllu@yzu.edu.cn.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Liu, K.; Harrison, M.T.; Yan, H.L.; Liu, D.L.; Meinke, H.; Hoogenboom, G.; Wang, B.; Peng, B.; Guan, K.Y.; Jaegermeyr, J.; et al. Silver lining to a climate crisis in multiple prospects for alleviating crop waterlogging under future climates. Nat. Commun. 2023, 14, 765. [Google Scholar] [CrossRef] [PubMed]
  2. Mustroph, A. Improving Flooding Tolerance of Crop Plants. Agronomy 2018, 8, 3390. [Google Scholar] [CrossRef]
  3. Kaur, G.; Vikal, Y.; Kaur, L.; Kalia, A.; Mittal, A.; Kaur, D.; Yadav, I. Elucidating the morpho-physiological adaptations and molecular responses under long-term waterlogging stress in maize through gene expression analysis. Plant Sci. 2021, 304, 110823. [Google Scholar] [CrossRef] [PubMed]
  4. Tian, L.X.; Bi, W.S.; Ren, X.S.; Li, W.L.; Sun, L.; Li, J. Flooding has more adverse effects on the stem structure and yield of spring maize (Zea mays L.) than waterlogging in Northeast China. Eur. J. Agron. 2020, 117, 126054. [Google Scholar] [CrossRef]
  5. Wang, X.W.; Li, X.Y.; Gu, J.T.; Shi, W.Q.; Zhao, H.G.; Sun, C.; You, S.C. Drought and waterlogging status and dominant meteorological factors affecting maize (Zea mays L.) in different growth and development stages in Northeast China. Agronomy 2023, 13, 374. [Google Scholar] [CrossRef]
  6. Huang, C.; Gao, Y.; Qin, A.Z.; Liu, Z.G.; Zhao, B.; Ning, D.F.; Ma, S.T.; Duan, A.W.; Liu, Z.D. Effects of waterlogging at different stages and durations on maize growth and grain yields. Agric. Water Manage 2022, 261, 107334. [Google Scholar] [CrossRef]
  7. Hu, J.; Yu, W.Z.; Liu, P.; Zhao, B.; Zhang, J.W.; Ren, B.Z. Responses of canopy functionality, crop growth and grain yield of summer maize to shading, waterlogging, and their combination stress at different crop stages. Eur. J. Agron. 2023, 144, 126761. [Google Scholar] [CrossRef]
  8. Ren, B.Z.; Yu, W.Z.; Liu, P.; Zhao, B.; Zhang, J.W. Responses of photosynthetic characteristics and leaf senescence in summer maize to simultaneous stresses of waterlogging and shading. Crop J. 2023, 11, 269–277. [Google Scholar] [CrossRef]
  9. Dash, S.S.; Lenka, D.; Sahoo, J.P.; Tripathy, S.K.; Samal, K.C.; Lenka, D.; Panda, R.K. Biochemical characterization of maize (Zea mays L.) hybrids under excessive soil moisture stress. Cereal Res. Commun. 2022, 50, 875–884. [Google Scholar] [CrossRef]
  10. Otie, V.; Ping, A.; Udo, I.; Eneji, E. Brassinolide effects on maize (Zea mays L.) growth and yield under waterlogged conditions. J. Plant Nutr. 2019, 42, 954–969. [Google Scholar] [CrossRef]
  11. Ren, B.; Zhang, J.; Dong, S.; Liu, P.; Zhao, B. Responses of carbon metabolism and antioxidant system of summer maize to waterlogging at different stages. J. Agron. Crop Sci. 2018, 204, 505–514. [Google Scholar] [CrossRef]
  12. Tian, L.X.; Li, J.; Bi, W.S.; Zuo, S.Y.; Li, L.J.; Li, W.L.; Sun, L. Effects of waterlogging stress at different growth stages on the photosynthetic characteristics and grain yield of spring maize (Zea mays L.) Under field conditions. Agric. Water Manag. 2019, 218, 250–258. [Google Scholar] [CrossRef]
  13. Ren, B.Z.; Dong, S.T.; Zhao, B.; Liu, P.; Zhang, J.W. Responses of nitrogen metabolism, uptake and translocation of maize to waterlogging at different growth stages. Front. Plant Sci. 2017, 8, 3389. [Google Scholar] [CrossRef] [PubMed]
  14. Alcázar-Alay, S.C.; Meireles, M.A.A. Physicochemical properties, modifications and applications of starches from different botanical sources. Food Sci. Technol. 2015, 35, 215–236. [Google Scholar] [CrossRef]
  15. Fan, H.Y.; Zhou, Z.Q.; Yang, C.N.; Jiang, Z.; Li, J.T.; Cheng, X.X.; Guo, Y.J. Effects of waterlogging on amyloplasts and programmed cell death in endosperm cells of Triticum aestivum L. Protoplasma 2013, 250, 1091–1103. [Google Scholar] [CrossRef] [PubMed]
  16. Zhou, Q.; Wu, X.J.; Xin, L.; Jiang, H.D.; Wang, X.; Cai, J.; Jiang, D. Waterlogging and simulated acid rain after anthesis deteriorate starch quality in wheat grain. Plant Growth Regul. 2018, 85, 257–265. [Google Scholar] [CrossRef]
  17. Zhou, Q.; Huang, M.; Huang, X.; Liu, J.; Wang, X.; Cai, J.; Dai, T.B.; Cao, W.X.; Jiang, D. Effect of post-anthesis waterlogging on biosynthesis and granule size distribution of starch in wheat grains. Plant Physiol. Biochem. 2018, 132, 222–228. [Google Scholar] [CrossRef]
  18. Arata, A.F.; Dinolfo, M.I.; Martinez, M.; Lazaro, L. Effects of waterlogging during grain filling on yield components, nitrogen uptake and grain quality in bread wheat. Cereal Res. Commun. 2019, 47, 42–52. [Google Scholar] [CrossRef]
  19. Li, H.W.; Wang, Z.S.; Zhuo, Q.C.; Zhang, B.; Wang, F.H.; Jiang, D. Starch granule size distribution and pasting characteristic response to post-anthesis combined stress of waterlogging and shading. Agriculture 2020, 10, 384. [Google Scholar] [CrossRef]
  20. Chen, Z.K.; Du, Y.F.; Mao, Z.L.; Zhang, Z.J.; Li, P.; Cao, C.G. Grain starch, fatty acids, and amino acids determine the pasting properties in dry cultivation plus rice cultivars. Food Chem. 2022, 373, 131472. [Google Scholar] [CrossRef]
  21. Xiong, R.Y.; Xie, J.X.; Chen, L.M.; Yang, T.T.; Tan, X.M.; Zhou, Y.J.; Pan, X.H.; Zeng, Y.J.; Shi, Q.H.; Zhang, J.; et al. Water irrigation management affects starch structure and physicochemical properties of indica rice with different grain quality. Food Chem. 2021, 347, 129045. [Google Scholar] [CrossRef] [PubMed]
  22. Zeng, R.; Chen, T.; Zhang, H.; Cao, J.; Li, X.; Wang, X.; Wang, Y.; Yao, S.; Gao, Y.; Chen, Y.; et al. Effect of waterlogging stress on grain nutritional quality and pod yield of peanut (Arachis hypogaea L.). J. Agron. Crop Sci. 2023, 209, 286–299. [Google Scholar] [CrossRef]
  23. Yu, X.R.; Yu, H.; Zhang, J.; Shao, S.S.; Xiong, F.; Wang, Z. Endospermstructure and physicochemical properties of starches from normal, waxy, and super-sweet maize. Int. J. Food Prop. 2015, 18, 2825–2839. [Google Scholar] [CrossRef]
  24. Lu, D.L.; Cai, X.M.; Lu, W.P. Effects of water deficit during grain filling on the physicochemical properties of waxy maize starch. Starch-Starke 2015, 67, 692–700. [Google Scholar] [CrossRef]
  25. Yang, H.; Wen, Z.R.; Huang, T.Q.; Lu, W.P.; Lu, D.L. Effects of waterlogging at grain formation stage on starch structure and functionality of waxy maize. Food Chem. 2019, 294, 187–193. [Google Scholar] [CrossRef] [PubMed]
  26. Lu, D.L.; Cai, X.M.; Shi, Y.X.; Zhao, J.R.; Lu, W.P. Effects of waterlogging after pollination on the physicochemical properties of starch from waxy maize. Food Chem. 2015, 179, 232–238. [Google Scholar] [CrossRef]
  27. Jiang, D.; Fan, X.M.; Dai, T.B.; Cao, W.X. Nitrogen fertiliser rate and post-anthesis waterlogging effects on carbohydrate and nitrogen dynamics in wheat. Plant Soil. 2008, 304, 301–314. [Google Scholar] [CrossRef]
  28. Yang, H.; Huang, T.Q.; Ding, M.Q.; Lu, D.L.; Lu, W.P. Effects of waterlogging around flowering stage on the grain yield and eating properties of fresh waxy maize. Cereal Chem. 2016, 93, 605–611. [Google Scholar] [CrossRef]
  29. Zheng, C.F.; Jiang, D.; Dai, T.B.; Jing, Q.; Cao, W.X. Effects of salt and waterlogging stress at post-anthesis stage on wheat grain yield and quality. Chin. J. Appl. Ecol. 2009, 20, 2391–2398. [Google Scholar]
  30. Zeng, R.E.; Chen, T.T.; Wang, X.Y.; Cao, J.; Li, X.; Xu, X.Y.; Chen, L.; Xia, Q.; Dong, Y.L.; Huang, L.P.; et al. Physiological and expressional regulation on photosynthesis, starch and sucrose metabolism response to waterlogging stress in peanut. Front. Plant Sci. 2021, 12, 601771. [Google Scholar] [CrossRef]
  31. Yang, H.; Shen, X.; Ding, M.Q.; Lu, D.L.; Lu, W.P. Effects of high temperature after pollination on grain development and endogenous hormone contents of waxy maize. J. Maize Sci. 2017, 25, 55–60. [Google Scholar]
  32. Hsieh, C.F.; Liu, W.C.; Whaley, J.K.; Shi, Y.C. Structure and functional properties of waxy starches. Food Hydrocolloids 2019, 94, 238–254. [Google Scholar] [CrossRef]
  33. Wu, A.C.; Gilbert, R.G. Molecular weight distributions of starch branches reveal genetic constraints on biosynthesis. Biomacromolecules 2010, 11, 3539–3547. [Google Scholar] [CrossRef] [PubMed]
  34. Chen, Y.; Yang, Q.; Xu, X.; Qi, L.; Dong, Z.; Luo, Z.; Lu, X.; Peng, X. Structural changes of waxy and normal maize starches modified by heat moisture treatment and their relationship with starch digestibility. Carbohydr. Polym. 2017, 177, 232–240. [Google Scholar] [CrossRef] [PubMed]
  35. Lu, D.L.; Guo, H.F.; Dong, C.; Lu, W.P. Starch granule size distribution and thermal properties of waxy maize cultivars in growing seasons. Acta Agron. Sin. 2010, 36, 1998–2003. [Google Scholar]
  36. Liu, L.M.; Klocke, N.; Yan, S.P.; Rogers, D.; Schlegel, A.; Lamm, F.; Chang, S.I.; Wang, D.H. Impact of deficit irrigation on maize physical and chemical properties and ethanol yield. Cereal Chem. 2023, 90, 453–462. [Google Scholar] [CrossRef]
  37. Li, S.; Xu, X.Z.; Guo, W.S.; Li, X.; Cheng, F. Study and application of negative pressure water supplying, controlling pot device and irrigation system. J. Shanghai Jiaotong Univ. (Agric. Sci.) 2008, 26, 478–482. [Google Scholar]
  38. Hansen, J.; Møller, I. Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal. Biochem. 1975, 68, 87–94. [Google Scholar] [CrossRef]
  39. GB/T 8885-2017; Edible Corn Starch—Code for Recommended National Standards. Standards Press of China: Beijing, China, 2017.
  40. Lin, L.S.; Guo, D.W.; Zhao, L.X.; Zhang, X.D.; Wang, J.; Zhang, F.M.; Wei, C.X. Comparative structure of starches from high-amylose maize inbred lines and their hybrids. Food Hydrocolloid 2016, 52, 19–28. [Google Scholar] [CrossRef]
  41. Cai, C.H.; Lin, L.S.; Man, J.M.; Zhao, L.X.; Wang, Z.F.; Wei, C.X. Different structural properties of high-amylose maize starch fractions varying in granule size. J. Agric. Food Chem. 2014, 62, 11711–11721. [Google Scholar] [CrossRef]
Plants 13 00108 g001
Figure 1. Effects of waterlogging at the flowering stage on grain yield and starch content of waxy maize. Mean value in the same column within each hybrid followed by different letters is significantly different (p < 0.05). SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging.
Figure 1. Effects of waterlogging at the flowering stage on grain yield and starch content of waxy maize. Mean value in the same column within each hybrid followed by different letters is significantly different (p < 0.05). SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging.
Plants 13 00108 g001
Plants 13 00108 g002
Figure 2. Effects of waterlogging at the flowering stage on the size distribution of waxy maize starch granules. SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging. The value in the bracket is the average granule size.
Figure 2. Effects of waterlogging at the flowering stage on the size distribution of waxy maize starch granules. SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging. The value in the bracket is the average granule size.
Plants 13 00108 g002
Plants 13 00108 g003
Figure 3. Effects of waterlogging at the flowering stage on molecular weight distribution of isoamylase debranched starch in waxy maize. SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging. Value in the bracket is the ratio of peak1 to peak2.
Figure 3. Effects of waterlogging at the flowering stage on molecular weight distribution of isoamylase debranched starch in waxy maize. SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging. Value in the bracket is the ratio of peak1 to peak2.
Plants 13 00108 g003
Plants 13 00108 g004
Figure 4. Effects of waterlogging at the flowering stage on X-ray diffraction pattern of waxy maize starch. SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging. Value in the bracket is the relative crystallinity.
Figure 4. Effects of waterlogging at the flowering stage on X-ray diffraction pattern of waxy maize starch. SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging. Value in the bracket is the relative crystallinity.
Plants 13 00108 g004
Table 1. Effects of waterlogging at the flowering stage on the flour pasting property of waxy maize.
Table 1. Effects of waterlogging at the flowering stage on the flour pasting property of waxy maize.
YearHybridWaterPV
(mPa·s)		TV
(mPa·s)		BD
(mPa·s)		FV
(mPa·s)		SB
(mPa·s)		Ptemp
(°C)
2014SYN5CK1384 ± 1 d1256 ± 6 a128 ± 7 d1660 ± 20 a404 ± 14 a76.1 ± 0.4 bc
WS998 ± 26 e927 ± 24 e71 ± 2 e1181 ± 32 e254 ± 8 de75.3 ± 0.4 c
YN7CK1378 ± 42 d1275 ± 34 a103 ± 8 d1692 ± 52 a417 ± 18 a76.1 ± 0.4 bc
WS1016 ± 2 e983 ± 3 de33 ± 1 f1299 ± 12 cd316 ± 9 b75.3 ± 0.4 c
2015SYN5CK1586 ± 20 b1134 ± 4 b452 ± 16 c1427 ± 6 b293 ± 2 bc77.9 ± 0.4 a
WS1477 ± 29 c1022 ± 22 cd455 ± 7 c1246 ± 22 de224 ± 0 e76.3 ± 0.4 bc
YN7CK1791 ± 4 a1075 ± 5 bc717 ± 9 a1344 ± 1 bc270 ± 6 cd76.3 ± 0.5 bc
WS1659 ± 13 b1061 ± 5 c599 ± 9 b1354 ± 9 bc293 ± 4 bc77.1 ± 0.4 ab
Mean value in the same column followed by different letters is significantly different (p < 0.05). SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging; PV, peak viscosity; TV, trough viscosity; BD, breakdown viscosity; FV, final viscosity; SB, setback viscosity; Ptemp, pasting temperature.
Table 2. Effects of waterlogging at the flowering stage on the flour thermal property of waxy maize.
Table 2. Effects of waterlogging at the flowering stage on the flour thermal property of waxy maize.
YearHybridWaterΔHgel
(J/g)		To
(°C)		Tp
(°C)		Tc
(°C)		ΔHret
(J/g)		%R
(%)
2014SYN5CK8.84 ± 0.24 abc69.6 ± 0.1 d75.6 ± 0.0 de82.4 ± 0.1 c3.5 ± 0.0 a39.7 ± 0.9 a
WS8.74 ± 0.22 bcd68.5 ± 0.1 e74.8 ± 0.0 f81.9 ± 0.1 c2.9 ± 0.1 b33.0 ± 0.3 b
YN7CK8.53 ± 0.12 cd70.2 ± 0.0 cd75.5 ± 0.0 e82.3 ± 0.0 c2.7 ± 0.2 b31.9 ± 1.5 b
WS8.23 ± 0.07 d68.3 ± 0.1 e74.6 ± 0.0 f83.1 ± 0.1 b2.1 ± 0.2 c24.9 ± 1.9 c
2015SYN5CK8.93 ± 0.07 abc72.5 ± 0.0 a77.8 ± 0.2 a84.7 ± 0.0 a3.6 ± 0.1 a40.8 ± 1.8 a
WS9.36 ± 0.11 a70.4 ± 0.1 cd76.2 ± 0.1 b83.3 ± 0.2 b4.1 ± 0.2 a43.2 ± 2.2 a
YN7CK8.83 ± 0.11 abcd71.4 ± 0.6 b76.0 ± 0.0 c82.9 ± 0.1 b3.6 ± 0.1 a40.6 ± 1.1 a
WS9.16 ± 0.30 ab70.9 ± 0.2 bc75.8 ± 0.2 cd83.0 ± 0.2 b3.7 ± 0.2 a40.0 ± 0.7 a
SYN5, Suyunuo5; YN7, Yunuo7; CK, control; WS, waterlogging; ΔHgel, gelatinization enthalpy; To, onset temperature; Tp, peak gelatinization temperature; Tc, conclusion temperature; ΔHret, retrogradation enthalpy; %R, retrogradation percentage. Mean value in the same column followed by different letters is significantly different (p < 0.05).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yang, H.; Cai, X.; Lu, D. Effects of Waterlogging at Flowering Stage on the Grain Yield and Starch Quality of Waxy Maize. Plants 2024, 13, 108. https://doi.org/10.3390/plants13010108

AMA Style

Yang H, Cai X, Lu D. Effects of Waterlogging at Flowering Stage on the Grain Yield and Starch Quality of Waxy Maize. Plants. 2024; 13(1):108. https://doi.org/10.3390/plants13010108

Chicago/Turabian Style

Yang, Huan, Xuemei Cai, and Dalei Lu. 2024. "Effects of Waterlogging at Flowering Stage on the Grain Yield and Starch Quality of Waxy Maize" Plants 13, no. 1: 108. https://doi.org/10.3390/plants13010108

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop