Plant anaerobic stress as a novel trend in ecological physiology, biochemistry, and molecular biology: 2. Further development of the problem

This review is a logical development of a previous publication, which summarized the main results of the early period of the systematic and active studying of hypoxic and anoxic stresses in plants. These studies laid a foundation for a new scientific discipline in biology, the investigation relevant to plant anaerobic stress. This review considers a further development of this trend when the investigations embraced a wider set of topics and the discipline acquired an international recognition. The results obtained during last decades by physiologists, biochemists, and molecular biologists engaged in the problem of plant anaerobic stress confirmed the correctness of a concept of the two principal strategies of plant adaptation to hypoxia and anoxia conditions. They are “true” tolerance manifesting at the molecular level under conditions of oxygen deficiency or its absence and “apparent” tolerance, which is realized by avoidance of anaerobiosis due to the long-distance oxygen transport. Therefore, experimental material available now is considered and discussed in this review mainly in the light of these principal notions. Especial attention is paid to the role of stress proteins, which synthesis is induced under hypoxia and anoxia. The results of these experiments confirmed earlier conclusions about the key role of energy (glycolysis and alcoholic fermentation) and carbohydrate (mobilization and utilization of reserved carbohydrates) metabolism in plant adaptation to oxygen deficiency or its absence from the environment. The phenomenon of hypoxic acclimation and its role in plant adaptation to anoxia are also considered. Along with these topics, a further development of pH-stat theory is discussed. A special attention is paid to plant strategy realized by the formation of the net of air-filled spaces (aerenchyma) and long-distance oxygen transport from aerated plant parts to those located in anaerobic environment (apparent tolerance). Among other important aspects, we consider (1) post-anaerobic plant injury by free oxygen radicals; (2) the physiological role of alternative pathways of plant adaptation (nitrate reduction and lipid synthesis); (3) the phenomenon of the adaptation syndrome in plants and possible molecular mechanisms of its realization; and (4) some biotechnological advances in the field of genetic and cell engineering used for the creation of plants more tolerant to anaerobic stress.     

Functional Electron Microscopy in Studies of Plant response and adaptation to Anaerobic Stress

This article reviews the contribution made by functional electronmicroscopy towards identifying and understanding the reactionsof plant roots and shoots to anaerobic stress. Topics examinedinclude: (1) unexpected hypersensitivity, rather than hyper-resistance,to anoxia of root tips of flooding-tolerant plants; (2) protective,rather than damaging, effects of a stimulated energy metabolism(glycolysis and fermentation) under anaerobic conditions; (3)the concept of two main strategies of plant adaptation to anaerobicenvironments, namely avoidance of anaerobiosis on the wholeplant level, termed ‘apparent’ tolerance, and metabolicadaptation at the cellular and molecular levels, termed ‘true’tolerance; (4) the importance of protein synthesis during hypoxiaand anoxia for enhanced energy production and metabolic adaptation;(5) a general adaptive syndrome in plants to stress at the ultrastructurallevel and a possible molecular mechanism for its realizationunder anoxia; (6) the physiological role of anaerobically synthesizedlipids and nitrate as alternative electron acceptors in an oxygen-freemedium; and (7) the selection of cell lines derived from calluscultures that possess enhanced tolerance to anoxia and can regeneratewhole plants with improved tolerance of soil waterlogging.     

Germination, seedling morphology and establishment of Cotnbretum bauchiense Hutch. & Dalz. (Combretaceae)

ONYEKWELU, S. S. C, 1990. Germination, seedling morphology and establishment of Cotnbretum bauchiense Hutch. & Dalz. (Combretaceae). Cotnbretum bauchiense is a suffrutex with short, erect, usually herbaceous stems arising from a woody root stock. It appears in savanna soon after fire and (lowers within a few weeks. The fruits germinate in 5–6 days. The germination is cryptogeal. On germination the true radicle and the apparent radicle formed by fused cotyledon stalks push down into the soil, carrying the plumule with them. The cotyledon lamina and part of the fused cotyledon stalks remain above the soil. Both the apparent radicle and the true radicle produce roots. Below the soil at the joint of the apparent radicle and the true radicle the plumule produces 1–3 shoots which grow out to the surface of the soil. The underground portion of the shoot bears scale leaves, from which the plant regenerates when the aerial shoot is damaged by fire. This type of germination is an adaptation that ensures successful establishment in an environment that is subjected to fire.     

Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective

Arbuscular mycorrhizal fungi (AMF) form widespread symbiotic associations with 80% of known land plants. They play a major role in plant nutrition, growth, water absorption, nutrient cycling and protection from pathogens, and as a result, contribute to ecosystem processes. Salinity stress conditions undoubtedly limit plant productivity and, therefore, the role of AMF as a biological tool for improving plant salt stress tolerance, is gaining economic importance worldwide. However, this approach requires a better understanding of how plants and AMF intimately interact with each other in saline environments and how this interaction leads to physiological changes in plants. This knowledge is important to develop sustainable strategies for successful utilization of AMF to improve plant health under a variety of stress conditions. Recent advances in the field of molecular biology, “omics” technology and advanced microscopy can provide new insight about these mechanisms of interaction between AMF and plants, as well as other microbes. This review mainly discusses the effect of salinity on AMF and plants, and role of AMF in alleviation of salinity stress including insight on methods for AMF identification. The focus remains on latest advancements in mycorrhizal research that can potentially offer an integrative understanding of the role of AMF in salinity tolerance and sustainable crop production.     

Tomato tolerance to abiotic stress: a review of most often engineered target sequences

Tomato is one of the most often cultivated vegetable species worldwide. Due to the anti-oxidative and anti-cancer properties of lycopene, tomato consumption as well as production is still increasing. However, its productivity is impaired by a wide range of abiotic stresses, and the establishment of stress-tolerant crops is a key challenge for agricultural biotechnology. Until now, a few genetic approaches have been used to achieve stress tolerance in cultivated tomato plants. Such achievements are based on current knowledge concerning plant adaptation. The presence of adverse environmental factors like extreme temperatures, salinity or drought cause definite biochemical and physiological consequences. Mostly, these are the changes in the metabolic pathways, the expression of stress-inducible genes or the accumulation of low-molecular compounds that play a crucial role in maintaining the plasticity of reactions. The biotechnological methods used to modify tomato to produce “upgraded” plants are based on introgression of several genes coding enzymes known to mitigate stress or genes contributing to signalling and diverse regulatory pathways. Here, we present an overview of the most often chosen target sequences/molecules that are genetically delivered or engineered to obtain tolerance to environmental constraints. Since adverse conditions cause interrelated stress responses, it is the tolerance molecular players that are consecutively presented in this paper rather than the typically reviewed division of stress types.     

Metabolic adaptation to flooding stress in upland and lowland rice seedlings

Ability of metabolic adaptation in upland and lowland rice (Oryza sativa L.) seedlings to flooding stress was compared. Flooding stress increased alcohol dehydrogenase (ADH) activity and ethanol concentration in shoots and roots of the upland and lowland rice seedlings. The difference in ADH activity and ethanol concentration in shoots between the upland and lowland rice was not apparent. However, both ADH activity and ethanol concentration in roots of the lowland rice were 2-fold greater than those in roots of the upland rice, suggesting that flooding-induction of ethanolic fermentation in lowland rice roots may be significantly greater than that in the upland rice roots. Since flooding often causes the anaerobic conditions in rooting zone than aerial part of plants and ethanolic fermentation is essential to survive in the anaerobic conditions, the ability of metabolic adaptation in lowland rice seedlings to flooding stress may be greater than that in upland rice seedlings.     

Large-scale de novo transcriptome analysis reveals specific gene expression and novel simple sequence repeats markers in salinized roots of the euhalophyte <Emphasis Type="Italic">Salicornia europaea</Emphasis>

Glycophytic plants suffer from severe stress and injury when roots are exposed to high salinity in the rhizosphere. In contrast, the euhalophyte Salicornia europaea grows well at 200 mM NaCl and can withstand up to 1000 mM NaCl in the root zone. Analysis of gene expression profiles and the underlying molecular mechanisms responsible for this tolerance have been largely overlooked. Using the Illumina sequencing platform and the short-reads assembly programme Trinity, we generated a total of 40 and 39 million clean reads and further 140,086 and 122,728 unigenes from the 200 mM NaCl and 0 mM NaCl treated tissues of S. europaea roots, respectively. All unigenes in this study were functionally annotated within context of the COG, GO and KEGG pathways. Unigene functional annotation analysis allowed us to identify hundreds of ion transporters related to homeostasis and osmotic adaptation as well as a variety of proteins related to cation, amino acid, lipid and sugar transport. We found significant enrichment in response to stress including the functional categories of “antioxidant activity”, “catalytic activity” and “response to stimuli”. These findings represent for a useful resource for the scientific community working on salt tolerance mechanisms. Conversely, a total of 8639 EST-SSRs from 131,594 unigenes were identified and 4539 non-redundant SSRs primers pairs were developed. These data provide a good foundation for future studies on molecular adaptation mechanisms of euhalophytes roots under saline environments and will likely facilitate the identification of critical salt tolerance traits to be transferred in economically important crops.     

Adaptations to Flooding Stress: From Plant Community to Molecule

Abstract: This review highlights four major topics in plant flooding research: the processes underlying vegetation zonation in the floodplain, the challenges of using model species to reveal adaptive responses in shoots and roots, the role of micro-organisms in flooded soils in relation to plant growth, and the molecular regulation of the hormone ethylene which is heavily involved in the adaptation reaction of flood-resistant plants. Model species and vegetation strategies are used to unravel mechanisms of vegetation zonation in the river flood-plain. In the case of woodlands, hydrological conditions determine to a large extent their zonation patterns under natural conditions. For softwood species, such as Salicaceae, the interaction between water levels and timing of seed dispersal is the dominating process determining their establishment success on river banks. Their strategy is well adapted to irregular, high and prolonged floods. Hardwood species, Quercus, Fraxinus, UImus and Acer, are flood-sensitive and inhabit the higher sites. They mainly have heavy seeds and germinate under shaded conditions. The most shade-tolerant hardwood species are the least well adapted to flooding. Anthropogenically influenced parts of the floodplain are characterized by grasslands with elevation level and management practices determining the species composition. Low-lying grasslands have flood-tolerant species; elevated zones are seldom flooded and have flooding-sensitive species. Following Grime (1998^[59]), plant species of major vegetation types within the floodplain zone can be divided into three categories–dominants, subordinates and transients–illustrating the diversity in plant species in relation to environmental properties. Model species that are indicative of the different conditions in the various zones are chosen to help in the understanding of morphological and physiological adaptations at the plant level. The formation of aerenchymatous roots and the capacity to elongate shoot parts upon submergence are among the main responses of surviving plants. The role of hormones in the adaptation reaction is emphasized. Owing to high porosities in roots of flood-tolerant plants, radial oxygen loss greatly influences nitrification and denitrification processes in the flooded soil. Nutrient cycles are restored by root-derived oxygen and the oxygenated rhizosphere is detoxified. A new development in flooding ecology is the unravelling of the molecular regulation of hormonally controlled processes. The expression of an ethylene receptor gene in Rumex palustris is highlighted. This paper ends with some suggestions for future flooding research.     

Growth Respiration of a Flood-Tolerant and a Flood-Intolerant Senecio Species: Correlation between Calculated and Experimental Values

Root growth respiration of Senecio aquaticus Hill (flood-tolerant) and Senecio jacobaea L. (flood-sensitive) was calculated, assuming different P: O ratios. The growth respiration values were calculated on the basis of the chemical composition of root and shoot dry matter, in combination with published data on the energy costs of biosynthetic and transport processes. The comparison between calculated and experimental values suggests a relatively low efficiency of ATP utilization in the roots of the flood-tolerant species. Root growth respiration of S. congestus (R.Br.)DC., which is also flood-tolerant, and Plantago lanceolata L. were also determined. The data showed that not all the flood-tolerant species investigated had high root growth respiration values. An “overflow model’ is proposed to explain observed differences in root growth respiration between species.     

Anaerobic metabolism enzymes as markers of flooding stress in maize seeds

Maize (Zea mays L.) seeds differ in their relative tolerance to the anaerobic environment caused by flooding. Seed tolerance to flooding stress depends on cellular and metabolic processes since gross anatomical responses have not developed at the pre-emergence stage. The study reported here characterizes the activities of four anaerobic respiratory enzymes: pyruvate decarboxylase (PDC), alcohol dehydrogenase (ADH), lactate dehydrogenase (LDH), and malic enzyme (ME) in the flood-tolerant A632 and floodsusceptible Mo 17 inbred maize seeds during flooding at 10 and 25°C. Each inbred consisted of two seed lots possessing 95% and 75% germination levels. Flooding increased the activities of all four enzymes. However, no consistent correlation between anaerobic enzyme activity and flood tolerance was observed across genotype, seed quality and flooding temperature. The results indicate that it may not be feasible to use whole-seed anaerobic enzyme activities to predict maize seed performance under flooding stress. Contribution from the Soil Drainage Research Unit, USDA-ARS, Columbus, OH, in cooperation with the Ohio Agricultural Research and Development Center, The Ohio State University. OARDC Journal Article No. 66–86.     

厌氧胁迫下芝麻不同耐渍基因型形态、生理及矿质元素变化的比较研究

在部控制氧下比较4种不同耐渍基因型芝麻的形态,生理指数及营养器官矿质元素含量变化。结果表明,耐渍品种种野芝7号与豫芝1号不定根条数增加4－5倍,净光合速率（Ph)下降幅度小,ADH活性增加约2倍,根据Ca,P含量显著升高,K降幅较小,根中其元素以及茎、叶中8种元素呈下降趋势。非耐渍品种丹巴格与遂平小籽黄,不定根条数无明显增加,Pn下降50％－60％,ADH活性可升高5－9倍;根中Ca,P含量亦增高,K下降较多,耐渍基因型有明显的结构适应特征,厌氧代谢的能量补偿作用相对次要,Ca,P在芝麻对厌氧胁迫的生理适应中起重要作用。     

Strigolactones in plant adaptation to abiotic stresses: An emerging avenue of plant research

Phytohormones play central roles in boosting plant tolerance to environmental stresses, which negatively affect plant productivity and threaten future food security. Strigolactones (SLs), a class of carotenoid‐derived phytohormones, were initially discovered as an “ecological signal” for parasitic seed germination and establishment of symbiotic relationship between plants and beneficial microbes. Subsequent characterizations have described their functional roles in various developmental processes, including root development, shoot branching, reproductive development, and leaf senescence. SLs have recently drawn much attention due to their essential roles in the regulation of various physiological and molecular processes during the adaptation of plants to abiotic stresses. Reports suggest that the production of SLs in plants is strictly regulated and dependent on the type of stresses that plants confront at various stages of development. Recently, evidence for crosstalk between SLs and other phytohormones, such as abscisic acid, in responses to abiotic stresses suggests that SLs actively participate within regulatory networks of plant stress adaptation that are governed by phytohormones. Moreover, the prospective roles of SLs in the management of plant growth and development under adverse environmental conditions have been suggested. In this review, we provide a comprehensive discussion pertaining to SL‐mediated plant responses and adaptation to abiotic stresses.     

Metabolic response of river birch and European birch and European birch roots to hypoxia

Flood tolerance of woody plants has been attributed to internal oxygen diffusion from shoot to root, metabolic adaptation within the root, or both. The purpose of this study was to compare several biochemical and physiological responses of birch roots to hypoxia in order to determine the nature of root metabolic adaptation to low oxygen tension. One-year-old seedlings of flood-tolerant river birch (Betula nigra L.) and flood-intolerant European birch (Betula pendula Roth) were transferred to solution culture, and the solutions were bubbled with air or nitrogen. After 18 days of hypoxia, total adenosine phosphate and ATP contents of river birch roots were 35% and 23% of controls, respectively, whereas those of European birch roots were 13% and 8%. Adenylate energy charge of river birch roots decreased between 6 and 12 days of hypoxia. In contrast, energy charge of European birch roots decreased after only 1 day of hypoxia. In vitro activity of cytochrome c oxidase and oxygen consumption capacity of excised roots from both birch species decreased under hypoxia. In vitro activity of alcohol dehydrogenase from roots of both species increased after 1 day of hypoxia. However, alcohol dehydrogenase activity from river birch roots increased 25-fold after 6 days of hypoxia, whereas that from European birch decreased back to control levels. Hypoxia decreased malate content of roots from both species. Metabolic adaptation within the root, rather than internal oxygen diffusion, appears to be responsible for the relative tolerance of river birch to hypoxia.     

Growth and development ofRumex roots as affected by hypoxic and anoxic conditions

The growth characteristics of threeRumex species were determined under different solution oxygen concentrations in hydroculture. These species all occur in a river foreland ecosystem and they were found to differ in their flood tolerance. The flood-tolerantR. maritimus undR. crispus developed a large number of new, aerenchymatous roots within a short period under low solution oxygen concentrations. Biomass production was not affected. In the flood-intolerantR. thyrsiflorus, however, only few slow-growing new roots were developed and biomass production was significantly reduced at solution oxygen concentrations below 2% (v:v). These different responses could be partly explained by a differential aerenchyma formation in new roots of the flood-tolerant species. Aerenchyma can relieve the oxygen stress of the root systems via internal aeration.The fast development of new roots of the flood-tolerantR. maritimus andR. crispus after the onset of anaerobiosis coincided with the reduction or cessation of growth of the primary roots. Notwithstanding the cessation of growth, however, primary roots of both species were able to recover following restoration of aerobic conditions after a 13-day anaerobic period. However, the roots ofR. thyrsiflorus ceased growing very soon after the onset of anaerobiosis. All had died within 10 days.The balance between the growth rates of the primary and the newly formed root system are discussed and related to the differential tolerance of theRumex species to transient flooding.     

Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research

Lorenz Hiltner is recognized as the first scientist to coin the term “rhizosphere” in 1904. His scientific career and achievements are summarized in this essay. Most of his research he performed in the Bavarian Agriculture–Botanical Institute (later named the “Bavarian Institute of Plant Growth and Plant Protection”) in Munich, where he was the director from 1902 to 1923. Beginning with intensive and thorough investigations on the germination and growth of different crop plants (legumes and non-legumes) Hiltner became convinced, that root exudates of different plants support the development of different bacterial communities. His definition of the “rhizosphere” in the year 1904 centered on the idea, that plant nutrition is considerably influenced by the microbial composition of the rhizosphere. Hiltner observed bacterial cells even inside the rhizodermis of healthy roots. In analogy with fungal root symbionts, Hiltner named the bacterial community that is closely associated with roots “bacteriorhiza.” In his rhizosphere concept, Hiltner also envisioned, that beneficial bacteria are not only attracted by the root exudates but that there are also “uninvited guests,” that adjust to the specific root exudates. Based on his observations he hypothesized that “the resistance of plants towards pathogenesis is dependent on the composition of the rhizosphere microflora.” He even had the idea, that the quality of plant products may be dependent on the composition of the root microflora. In addition to his scientific achievements, Hiltner was very dedicated to applied work. Together with F. Nobbe he had the first patent on Rhizobium inoculants (Nitragin). He continuously improved formulations and the effectivity of the Rhizobium preparations and he also initiated seed dressing with sublimate for plant protection of seedlings. Thus, Hiltner tightly linked breakthroughs in basic research to improved rhizosphere management practices. In addition, he wrote a pioneering monograph on plant protection for everybody’s practical use. His emphasis on understanding microbes in the context of their micro-habitat, the rhizosphere, made him a pioneer in microbial ecology. Even now, in the era of genome and postgenome analysis with our better understanding of plant nutrition and soil bacteriology, his ideas and contributions are as fresh as they were more than 100 years ago.     

PGPR regulate caspase-like activity,programmed cell death,and antioxidant enzyme activity in paddy under salinity

The response of two root associated bacteria Pseudomonas pseudoalcaligenes and Bacillus pumilus were studied in the (salt-sensitive) rice GJ17 cultivar to salinity under controlled environmental growth conditions for protection of plant from adverse effect of salinity. Salinity affects the growth of salt-sensitive cultivar, but inoculation of plant growth promoting rhizobacteria (PGPR) reduces the harmful effect of salinity. The present study states that PGPR helps to reduce lipid peroxidation and superoxide dismutase activity in salt-sensitive GJ17 cultivar under salinity and play an important role in the growth regulation for positive adaptation of plants to salt stress. This study shows that inoculation of paddy (Oryza sativa) with such bacteria could provide salt-tolerant ability by reducing the toxicity of reactive oxygen species by reducing plant cell membrane index, cell caspase-like protease activity, and programmed cell death and hence resulted in increase cell viability. As these isolates remain associated with the roots, the effects of tolerance against salinity are observed here. Results also indicate that isolated PGPR strain help in alleviating up to 1.5 % salinity stress as well as improve tolerance.     

Tracking changes in life‐history traits related to unnecessary virulence in a plant‐parasitic nematode

Evaluating trade‐offs in life‐history traits of plant pathogens is essential to understand the evolution and epidemiology of diseases. In particular, virulence costs when the corresponding host resistance gene is lacking play a major role in the adaptive biology of pathogens and contribute to the maintenance of their genetic diversity. Here, we investigated whether life‐history traits directly linked to the establishment of plant–nematode interactions, that is, ability to locate and move toward the roots of the host plant, and to invade roots and develop into mature females, are affected in Meloidogyne incognita lines virulent against the tomato Mi‐1.2 resistance gene. Virulent and avirulent near‐isogenic lines only differing in their capacity to reproduce or not on resistant tomatoes were compared in single inoculation or pairwise competition experiments. Data highlighted (1) a global lack of trade‐off in traits associated with unnecessary virulence with respect to the nematode ability to successfully infest plant roots and (2) variability in these traits when the genetic background of the nematode is considered irrespective of its (a)virulence status. These data suggest that the variation detected here is independent from the adaptation of M. incognita to host resistance, but rather reflects some genetic polymorphism in this asexual organism.     

Supply and partitioning of assimilates to roots of Medicago sativa L. and Lotus corniculatus L. under anoxia

Abstract A current explanation of the mechanism of flooding injury to roots suggests that oxygen deficiency depresses the supply of respirable carbohydrates sufficiently to inhibit fermentation. However, even though it has been shown that phloem transport of assimilate is sharply reduced to anaerobic roots, inhibition of assimilate metabolism has also been suggested to be an important factor. This study examines these hypotheses by relating assimilate supply and metabolic activity in anoxic roots of alfalfa (Medicago sativa L.), a flood-intolerant species, and birdsfoot trefoil (Lotus corniculatus L.), a flood-tolerant plant. Roots were made anoxic (severe O₂ deficiency) for 2, 4 or 6 d and shoots were labelled with ¹⁴CO₂. Assimilate transport to the roots and metabolism to structural components were significantly decreased in both species in response to anoxia. Trefoil exhibited significantly greater ¹⁴C incorporation into the residue fraction at 4 d anoxia than did alfalfa, and this was consistent with the greater flooding tolerance of trefoil. When assimilate supply to O₂-deficient roots was decreased by shoot shading, shoot fresh weight was reduced by both anoxia and light treatments. Root-soluble sugars were significantly decreased by shading but were greatly increased in response to anoxia. Root starch concentration also increased under anoxia. Root K⁺ concentration was reduced by anoxia only. The energy status (ATP/ADP) of roots was significantly decreased by shading; however, anoxia reduced the energy status only in unshaded plants. The data indicate that carbohydrate supply to anaerobic roots does not appear to be a limiting factor in the metabolic response of alfalfa roots. Alternatively, metabolism of assimilate in anoxic roots may be an important determinant of survival.