How environmental stress affects starch composition and functionality in cereal endosperm

TL;DR: Variations in soil moisture and nutrient availability, ambient temperature, and atmospheric composition were all shown to affect starch functionality and Genotypic variation appears to be a primary contributor for the response of cereal starches to environmental stress.

Abstract: Stressful environments can alter starch biosynthesis in cereal endosperm. The aim of this review is to carefully examine how starch functional properties are altered when plants encounter environmental parameters outside of the normal range. This is important because while growers and processors require grain yield stability and product uniformity this will be challenging in an era of variable weather patterns. Being able to predict the general physico-chemical nature of the starch as a result of growth status is a step towards the precise agriculture required for the 21st century. Variations in soil moisture and nutrient availability, ambient temperature, and atmospheric composition were all shown to affect starch functionality. Elevated temperature led to the most significant changes in both tropical and temperate cereals and amylose content was the most sensitive parameter under various environmental conditions. Genotypic variation appears to be a primary contributor for the response of cereal starches to environmental stress. Nonetheless, while a large amount of data from single controlled environmental stress experiment is currently available, comparably little is known about whether similar results would be achieved in multifactorial and large-scale settings. The challenges in terms of the need for more detailed experimental descriptions to lessen the study-to-study discrepancies of data and to enhance their interpretability were also discussed. © 2013 WILEY-VCH Verlag GmbH and Co. KGaA, Weinheim.

Summary

1 Introduction

• The amount, composition, and uniquemolecular structure of modern-day commercial cereal starches are the result of careful agricultural management [1] combined with 1000s of years of selection for desirable germplasm [2–6].
• In addition, there has been a recent and intense focus on predicting how environmental changes will affect agricultural productivity and the quality of food [23].
• This review seeks to update their current knowledge in the field.

2 Starch structure and composition

• Starch is the main carbon reserve in cereal endosperm, accounting for 50–90% of dry matter in the tissue [24–28].
• It is deposited as discrete particles, of which the size, morphology, and relative numbers are strongly dependent on genetic, developmental, and environmental factors [25, 29, 30].
• For a more comprehensive understanding of starch molecular structure and composition, readers are referred to these reviews [27, 33], as only a brief description will be given here.
• The branching in amylopectin is defined, and leads to a recognizable pattern of glucan chains of defined lengths arrayed into alternating concentric crystalline and amorphous lamellae [33, 36, 37].

3 Relationship between starch structure and functionality

• The functional behavior of starch is intricately linked to its structure and morphology.
• Changes in the proportion of amylose to amylopectin, glucan chain length distribution, degree of crystallinity, or granule size distribution can alter starch physico-chemical characteristics [31].
• The ensuing solid-gel phase transitions in large part determine texture and eating quality attributes [31].
• To assess starch functionality, parameters such as starch swelling power, viscosity, gelatinization, and retrogradation are used to predict potential applications and quality [10].

3.1 Starch swelling power

• At the onset of starch gelation, water ingresses into the granules, making them “swell.”.
• The swelling pattern occurs in two phases, first in the amorphous core of the granule, and second in the semicrystalline lamellae when most of the amylose molecules have leached out of the granules [41, 43, 44].
• The presence of the amylose-lipid complex and the aggregated amylose molecules is responsible for restraining swelling events [39, 41].
• Small granules were found to have higher water absorbability compared to the large granules, due potentially to the differences in the way the glucan chains are ordered [45], and the higher surface area per unit weight of the small granules [46, 47].

3.2 Starch viscosity

• Viscosity occurs during gelatinization when, mainly, amylose leaches from the starch granule and forms a matrix on the exterior surface of the granule [31, 39].
• Paste viscosity reaches its maximumwhen all granules are swollen, but still intact [31, 49], and once the granules break down and the polysaccharides become dispersed in the medium, the paste viscosity diminishes [31].
• Starch with low amylose content will have high peak viscosity [31, 50], and low setback viscosity, reflecting the diminished amylose gel network [50].
• Smaller granules have lower peak viscosity and breakdown, but higher peak viscosity temperature in comparison to the larger granules [51].

3.3 Starch Gelatinization

• Gelatinization is described as the phase transition of the starch granule in the presence of heat and excess plasticizer, typically water [41].
• The internal structure of the granule breaks down, leading to granule disassembly and leaching of the polysaccharides into the medium [52].
• An irreversible loss of crystallinity only occurs when the temperature reaches the threshold where both the interactions among the neighboring amylopectin side-chains and between the side-chains of the double helices are lost [53].
• This temperature is, however, varied according to the composition of starch [50] and the abundance of water [54, 55].
• Starches with higher proportions of long amylopectin sidechains [50], greater amount of amylose-lipid complexes [50], or smaller granules [45, 47] exhibit low gelatinization temperatures.

3.4 Starch retrogradation

• Retrogradation of gelatinized starch occurs when the amylose and amylopectin molecules realign and interact to create more crystalline molecules as the starch cools [59].
• This negatively affects the storage [41] and freeze-thaw stability [48] of starch in industrial applications.
• Low amylose content [53, 60], high proportions of small side-chains amylopectin [41], low lipid content [50], and large granule size [47] prevent starch from retrograding.

4 Effect of the environment on starch structure and functionality

• Starch functionality is in turn affected by, in addition to genotypes, growing season temperature, rainfall patterns and humidity, growth locations, and sustained or episodic environmental stresses [61].
• These enzymes form interdependent complexes that cooperatively synthesize starch [73, 74].
• Changes in the spectrum of enzymes in these complexes will substantially alter the structure and composition of the granules [15].
• The readers are referred to the recent review [15] on the topic for more detailed information.

4.1 Temperature extremes

• Temperature has long been known as a critical element determining agricultural productivity.
• Future climatic predictions all suggest that on average, higher temperatures will be the new norm [22] and as a result, the effect of elevated temperatures on crop productivity has been extensively studied [17].
• An interesting but neglected corollary is that higher temperatures in some regions can be directly linked to a cooling trends in other regions [75], and crops in the latter areas may be increasingly subjected to chilling stress.

4.1.1 Heat

• High air and soil temperatures are the primary stressors that reduce grain starch production and alter starch functionality [16, 76, 77].
• High growth temperature decreased amylose content in maize [79] and increased it in wheat [80–86], but the magnitude of these changes were neither as significant nor as consistent compared to Japonica rice where amylose may be reduced as much as 20% at temperatures above 30 °C [87–95].
• Conversely, the trend in wheat is toward the accumulation of shorter glucan chains [82, 83], while a single report for sorghum suggests it responded similarly to rice [104].

4.1.2 Cold

• Generally, there were increases in the ratio of amylose to amylopectin in the grain of rice grown in controlled low temperature environments [114], cooler field locations [69], and colder seasons [61].
• There have not been many in-depth analyses of starch functionality on cold-treated cereals, nonetheless, gelatinization and pasting temperatures generally decreased in most [69, 121] but not all [118] studies.
• In the field study by Dang and Copeland [61], several rice cultivars had a lower peak viscosity and greater setback of the rice flour when ambient temperatures were reduced.
• These starches also showed greater amylolysis in vitro, indicating changes in the molecular structure of starch [121].

4.2 Soil moisture and nutrient composition

• Soil physical structure, osmotic properties, and chemical composition can influence grain starch.
• Cereal production in many regions is still rain-fed [123].
• Poor agricultural management of soils and high radiation together are increasing soil salinity [124].
• Increasing social, political, and economic pressures to reduce chemical inputs for agriculture suggests that growers will be more judicious in terms of the rates and amounts of fertilization applied.
• How these elements change grain starch properties are considered in this section.

4.2.1 Water deficit

• Inducing a moderate water deficit in cereals can cut starch accumulation by up to 40%, leading to changes in starch composition, structure, and functionality [15].
• Rain-fed wheat with variable watering through development and overall lower soil moisture content compared with that of the irrigated control, had a higher proportion of B- and fewer Agranules, suggesting the timing of the stress may also be critical [125].
• Starch granule size distribution in barley endosperm was more resilient with changes only evident under long-term water stress, following a similar pattern to that seen in wheat [132, 136, 137].
• Restricting watering to rice and wheat was shown to alter starch functionality, especially the pasting properties.
• There was also an increase in grain chalkiness and milling properties in another study [131].

4.2.2 Salinity

• Salinity stress effects on starch functionality have been studied in rice and triticale.
• Rice is highly sensitive to saline soil but the response is not influenced by the salt-sensitivity of the cultivar [138, 139].
• There also appears to be great genetic variability for this trait [138, 139], and the type of salt used may have a greater effect on starch structure than the salt concentration [138].
• Apparent amylose content in IR5929 was not affected, but gelatinization temperature was lower under all salt concentrations [138].
• At 100 and 200mM sodium choride the granules surface was studded with indentations [140].

4.2.3 Nitrogen deficiency

• Variation in soil nitrogen (N) usually has direct consequences for the starch-to-protein ratio in grain, which would suggest ramifications for starch functionality [141], although several studies demonstrated that the effect on starch is unpredict- able [142].
• Wang et al. [148] found that lower N increased amylose in wheat but this effect could be reversed, i.e., amylose increased, if the wheat was also irrigated at a higher frequency.
• Gelatinization parameters are not greatly impacted in some studies [144, 145], but in another study, both transition temperatures and enthalpy of gelatinization were reduced [146].
• While these changes were measurable, genotypes and other interacting environmental factors reduced the severity of the impact of nitrogen deficiency [149, 150, 155].

4.3 Atmospheric composition

• The relative proportion of CO2, O3, and other pollutants in the atmosphere continues to increase and this is anticipated to have repercussions for grain productivity [156, 157].
• The cultivar used, the concentration of CO2 and O3, mode of delivery, duration of exposure, crop developmental stage, as well as general environmental conditions may, in concert, lead to a wide range of alterations in starch properties [15].
• Elevated CO2 and O3 are predicted to have opposing effects, with the former improving yield and the latter decreasing it [158, 159].
• Such alterations would presumably, by extension, affect starch composition and functionality.

4.3.1 Elevated CO2

• How higher than normal CO2 affects cereal starch shows little commonality even within species [15].
• Madan et al. [96] exposed three distinct rice cultvars to the same concentration of CO2 and found that only one of the three cultivars had changes in amylose content [96], supporting the genetic background as a major contributory factor.
• This suggests that CO2 concentration was the primary determinant of the differential effect in Hartog, though this may be an oversimplification.
• When Hartog was compared with another cultivar Rosella at 900 ppmCO2 [161], the latter did not change in granule distribution, again indicating that genotype is playing a major role in the variable results shown in wheat.
• Notably, very few studies have been done in other cereals besides rice; however, changes in starch functionality to high CO2 in this species showed little consistency [162].

4.3.2 Elevated O3

• There are very limited accounts of how higher O3 affects grain starch.
• Of the three published studies available, there was no change in the amount of starch accumulated in thewheat grain in one study [171], while it decreased in the other studies in wheat and rice [159, 172].
• The most extensive study on how O3 affects starch functionality was done in rice [179].
• Plants were exposed to 5% v/v O3, which is 25% higher than ambient level, using free-air gas concentration enrichment in two consecutive years [179].
• Amylose was only reduced in 1 year, while gel consistency remained unchanged [179].

5 Challenges in understanding the effect of environments on starch functionality

• There have been great discrepancies in the data reported from different studies, and their interpretation should be done with caution because they may be due to extraneous factors, independent of the applied environmental stress [16].
• Comparing a wide array of cereal genotypes at divergent developmental stages would be expected to generate significant differences among the data observed.
• In addition, variations in treatment concentration, period (long-term vs. short-term stress), time of application, as well as treatment stability are crucial for determining grain starch composition and functionality.
• Since reproducing similar experimental conditions in individual laboratories, greenhouses, or chambers is likely to be impossible, recording and reporting the environmental variables that the plants were exposed to would be important for data interpretation and comprehensibility.
• The authors wish to emphasize some interactors that could have profound effects on starch functionality, and could come into question when interpreting the environmental stress experimental data.

5.1 Crop genetic variations

• Most of the work the authors have reviewed here showed that genotypic background is a critical contributory factor for starch functionality parameters [103, 123, 150, 180].
• Some genotypes may vary in their inherent resistance to abiotic stress.
• There may be differences in the spectrum of starch biosynthetic enzymes tolerant of poor conditions.
• Studying how the starch in cultivars with contrasting compositional and structural features (e.g., waxy vs. nonwaxy starches) changes when grown under stress may offer novel insight into starch chemistry and biology [103].
• Studying how a broad spectrumof cereal genotypes from highly tolerant to highly sensitive types responds to stressmay also inform on the mechanisms for maintaining granule stability.

5.2 Grain developmental stages

• The effect of extreme environments is generally greatest during grain initiation and early grain filling due to the interference of sensitive cell physiological and biochemical 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.starch-journal.com processes required for organ establishment and starch biosynthetic activity [15].
• Measurable changes were pronounced at late grain filling, and could be the accumulated effect from the earlier stages [127, 181, 182].
• Time-course treatment regimes would help to pinpoint the interaction of the treatment and plant developmental stages [109].
• For rice, a precise growth and developmental staging system was invented to improving communication between researchers, growers, and educators [183].

5.3 Extraneous factors

• The circumstances faced by plants during their growth often affects physiological and biochemical processes, and may either maximize or lessen the observed changes in starch composition and functionality due to the treatment effect.
• This could be problematic when the array of phenotypes, which could be potentially observed, is masked by variation in growing environments.

5.3.1 Light

• Both the source and intensity of light can influence starch deposition.
• In barley, mercury lamps gave lower light intensity compared with sodium lamps, and this led to unexpected differences in starch such as, the abolition of diurnal growth rings in the granule, modulations in amylose, and granule numbers and size [117].
• Low light intensity also changed granule size distribution in wheat [184], and decreased viscosity parameters in waxy maize starch [185].

5.3.2 Diurnal temperature

• Both elevated day-time temperature alone [98–100] and elevated day- and night-time temperatures [93, 95, 186] at grain filling have been long shown to affect rice starch composition and cooking properties.
• Elevated NTAT alone was recently proved to significantly affect rice grain qualities both in the field [182] and in controlled environmental growth conditions [187].
• The importance of elevated NTAT on rice grain quality was insightfully emphasized in a recent review [14].

5.3.3 Soil temperature

• Guedira et al. showed that high temperature applied to root caused alterations in grain starch quality, distinct from the degree and compositional aspects recorded when high temperature was applied to the shoot [188].
• This points to the notion that the soil temperature measurement should be taken into account when designing temperature stress experiments.

5.3.4 Irrigation regime

• A water-saving irrigation regime altered several grain quality parameters in comparison to the conventional irrigation in China [131].
• The same was found in wheat in studies where there were differences in the periodicity of watering [119, 125].
• Therefore, the way plants are irrigated influences grain starch functionality experiment.

5.4 Combinatorial stresses

• Most studies examining the environmental effects on cereal starch functionality have focused on a single type of stress, while in the field, the plants are likely to be concurrently exposed to several types of stresses, which may pose more confounding effects on grain biosynthetic processes [191].
• It is often difficult to predict the effect of combinatorial stress based on the effects seen when each stress is individually applied.
• Nonetheless, in another combinatorial study, wheat starch content and thermal property were strongly affected by elevated temperature, with very little effect when CO2 concentration was increased in concert [84].
• This should encourage more investigation of the impact from various stress combinations on starch functionality in all major cultivated cereals in spite of the associated expenses.

5.5 Field studies

• Stress studies conducted in controlled-environment greenhouses or chambers may or may not yield the same degree of alterations in kernel starch composition and functionality if conducted in a field experiment.
• A study of 27 rices cultivars grown in the cold and hot regions in the US yielded the same findings in terms of starch composition and thermal properties when compared to the non-field studies conducted by other researchers [69].
• Nevertheless, triticale grain starch was not significantly influenced by locations, rather, cultivars and growing year made a remarkable impact [142].
• Extrapolating data from non-field studies to large-scale and long-term cereal cultivation in the fields may not be accurate and more of the field-type stress studies are required to ensure the applicability of the stress research data to commercial settings.

6 Conclusions

• Starch structure is directly related to its physico-chemical property, which largely determines its quality in downstream applications.
• This coud be explained by the variations in several experimental factors mentioned above.
• The combinatorial nature of environmental extremes plants are confronted with in the fields also adds to the need for both multiple stresses treatment and field studies.
• Acquiring a more comprehensive understanding of how the environment affects starch quality could help both local and international growers, and industrial sectors to come to terms with how “stressed starch” could be utilized and marketed in this era of variable climatic patterns.
• The authors have declared no conflict of interest.

Frequently asked questions

Q1. What are the contributions mentioned in the paper "How environmental stress affects starch composition and functionality in cereal endosperm" ?

A comprehensive review of the current knowledge in the field can be found in this paper, where Maysaya Thitisaksakul and Diane M. Beckles provide a comprehensive overview of the state-of-the-art. 

Q2. What are the future works in "How environmental stress affects starch composition and functionality in cereal endosperm" ?

While there is a need of comprehensive understanding of how starch functionality is affected by certain environmental extremes, there are discrepancies in the current knowledge due to variations from study to study.