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1.  Differences in responses to flooding by germinating seeds of two contrasting rice cultivars and two species of economically important grass weeds 
AoB Plants  2014;6:plu064.
Barnyard grasses are serious weeds in direct seeded rice. We assessed the effectiveness of using controlled flooding for its control using two rice cultivars and two barnyard grasses contrasting in flood tolerance during germination. Flooding with 100 mm water after seeding suppressed barnyard grasses; but delaying flooding by 2-4 days was ineffective. Flooding increased the activity of alcohol dehydrogenase and pyruvate decarboxylase; the increase was higher in the tolerant rice cultivar but similar in both barnyard grasses. Aldehyde dehydrogenase activity increased only in flood-tolerant types of rice and weeds, but not in flood-sensitive types, implying potential role in tolerance.
Crop productivity is largely affected by abiotic factors such as flooding and by biotic factors such as weeds. Although flooding after direct seeding of rice helps suppress weeds, it also can adversely affects germination and growth of rice, resulting in poor crop establishment. Barnyard grasses (Echinochloa spp.) are among the most widespread weeds affecting rice, especially under direct seeding. The present work aimed to establish effective management options to control these weeds. We assessed the effects of variable depths and time of submergence on germination, seedling growth and carbohydrate metabolism of (i) two cultivars of rice known to differ in their tolerance to flooding during germination and (ii) two barnyard grasses (Echinochloa colona and E. crus-galli) that commonly infest rice fields. Flooding barnyard grasses with 100-mm-deep water immediately after seeding was effective in suppressing germination and growth. Echinochloa colona showed greater reductions in emergence, shoot and root growth than E. crus-galli. Delaying flooding for 2 or 4 days was less injurious to both species. Echinochloa colona was also more susceptible to flooding than the flood-sensitive rice cultivar ‘IR42’. The activity of alcohol dehydrogenase (ADH) and pyruvate decarboxylase (PDC) in rice seedlings was increased by flooding after sowing but with greater increases in ‘Khao Hlan On’ compared with ‘IR42’. The activity of ADH and PDC was enhanced to a similar extent in both barnyard grasses. Under aerobic conditions, the activity of ADH and PDC in the two barnyard grasses was downregulated, which might contribute to their inherently faster growth compared with rice. Aldehyde dehydrogenase activity was significantly enhanced in flood-tolerant ‘Khao Hlan On’ and E. crus-galli, but did not increase in flood-sensitive E. colona and ‘IR42’, implying a greater ability of the flood-tolerant types to detoxify acetaldehyde generated during anaerobic fermentation. Confirmation of this hypothesis is now being sought.
doi:10.1093/aobpla/plu064
PMCID: PMC4243074  PMID: 25336336
Alcohol dehydrogenase; aldehyde dehydrogenase; anaerobic germination; barnyard grass; direct-seeded rice; Echinochloa colona; Echinochloa crus-galli; fermentative metabolism; pyruvate decarboxylase; rice weeds.
2.  Seed pre-treatment in rice reduces damage, enhances carbohydrate mobilization and improves emergence and seedling establishment under flooded conditions 
AoB Plants  2011;2011:plr007.
Priming rice seeds (soaking followed by drying) or soaking just before sowing improved emergence from flooded soil, reduced membrane damage from ROS and hastened carbohydrate mobilization. Most benefit was to lines with a superior ability to germinate in flooded soil even when untreated.
Background and aims
Early flooding helps control weeds but reduces seedling establishment in direct-seeded rice (Oryza sativa). When combined with appropriate management practices, the use of genotypes that better tolerate flooding during emergence can enhance crop establishment in flood-prone areas. Management options include seed pre-treatment and we tested the influence of pre-soaking for 24 h prior to sowing or of priming (soaking for 24 or 48 h followed by drying).
Methodology
The effects on seedling establishment after 21-day flooding of pre-soaking seeds for 24 h before sowing and/or of priming seeds were examined together with physiological responses connected with reactive oxygen scavenging. Seeds of four lines with contrasting abilities to tolerate flooding at the germination stage were compared. Seeds were primed using KCl solutions (48 h) or water (24 h) and pre-soaked using water. Lipid peroxidation and activities of reactive oxygen-scavenging enzymes were measured in seeds before sowing. Carbohydrate mobilization in germinating seeds and seedling growth were also monitored at intervals.
Principal results
Seed pre-treatment by pre-soaking or by priming increased survival of flooding and accelerated and improved seedling establishment, especially in tolerant genotypes. Primed seeds had less lipid peroxidation and higher superoxide dismutase (SOD) and catalase (CAT) activities than non-primed seeds. Amylase activities and starch breakdown were also hastened in primed seeds. Survival after flooding was positively correlated with amylase activity but negatively correlated with the extent of lipid peroxidation.
Conclusions
Pre-soaking and priming improved seedling establishment in flooded soil, enhanced the capacity to scavenge reactive oxygen species in seeds by increasing SOD and CAT activities, and hastened carbohydrate mobilization. Tolerant genotypes responded better to these treatments, emphasizing the effectiveness of combining genetic tolerance with appropriate seed pre-treatment to improve seedling establishment of rice sown in flooded soils.
doi:10.1093/aobpla/plr007
PMCID: PMC3072768  PMID: 22476478
3.  Seed Germination Ecology of Echinochloa glabrescens and Its Implication for Management in Rice (Oryza sativa L.) 
PLoS ONE  2014;9(3):e92261.
Echinochloa glabrescens is a C4 grass weed that is very competitive with rice when left uncontrolled. The competitive ability of weeds is intensified in direct-seeded rice production systems. A better understanding is needed of factors affecting weed seed germination, which can be used as a component of integrated weed management in direct-seeded rice. This study was conducted to determine the effects of temperature, light, salt and osmotic stress, burial depth, crop residue, time and depth of flooding, and herbicide application on the emergence, survival, and growth of two populations [Nueva Ecija (NE) and Los Baños (IR)] of E. glabrescens. Seeds from both populations germinated at all temperatures. The NE population had a higher germination rate (88%) from light stimulation than did the IR population (34%). The salt concentration and osmotic potential required to inhibit 50% of germination were 313 mM and −0.24 MPa, respectively, for the NE population and 254 mM and −0.33 MPa, respectively, for the IR population. Emergence in the NE population was totally inhibited at 4-cm burial depth in the soil, whereas that of the IR population was inhibited at 8 cm. Compared with zero residue, the addition of 5 t ha−1 of rice residue reduced emergence in the NE and IR populations by 38% and 9%, respectively. Early flooding (within 2 days after sowing) at 2-cm depth reduced shoot growth by 50% compared with non-flooded conditions. Pretilachlor applied at 0.075 kg ai ha−1 followed by shallow flooding (2-cm depth) reduced seedling emergence by 94−96% compared with the nontreated flooded treatment. Application of postemergence herbicides at 4-leaf stage provided 85−100% control in both populations. Results suggest that integration of different strategies may enable sustainable management of this weed and of weeds with similar germination responses.
doi:10.1371/journal.pone.0092261
PMCID: PMC3958481  PMID: 24642568
4.  Adaptation to flooding in upland and lowland ecotypes of Cyperus rotundus, a troublesome sedge weed of rice: tuber morphology and carbohydrate metabolism 
Annals of Botany  2008;103(2):295-302.
Background and aims
In recent years, Cyperus rotundus has become a problem weed in lowland rice (Oryza sativa) grown in rotation with vegetables in the Philippines. As the growth of C. rotundus is commonly suppressed by prolonged flooding, the ability of the weed to grow vigorously in flooded as well as upland conditions suggests that adapted ecotypes occur in these rotations. Studies were conducted to elucidate the mechanisms that permit C. rotundus to tolerate flooded soil conditions.
Methods
Upland and lowland ecotypes of C. rotundus were compared in terms of growth habit, carbohydrate reserves and metabolism, and activities of enzymes involved in alcoholic fermentation – alcohol dehydrogenase (ADH) and pyruvate decarboxylase (PDC).
Key Results
The lowland ecotype has much larger tubers than the upland ecotype. Prior to germination, the amylase activity and total non-structural carbohydrate content in the form of soluble sugars were greater in the tubers of lowland plants than in those of upland C. rotundus. At 24 h after germination in hypoxic conditions, PDC and ADH activities in the lowland plants increased, before decreasing at 48 h following germination. In contrast, ADH and PDC activities in the upland plants increased from 24 to 48 h after germination.
Conclusions
Tolerance of lowland C. rotundus of flooding may be attributed to large carbohydrate content and amylase activity, and the ability to maintain high levels of soluble sugars in the tubers during germination and early growth. This is coupled with the modulation of ADH and PDC activities during germination, possibly to control the use of carbohydrate reserves and sustain substrate supply in order to avoid starvation and death of seedlings with prolonged flooding.
doi:10.1093/aob/mcn085
PMCID: PMC2707299  PMID: 18515404
Anoxia; ethanol fermentation; flooding tolerance; nutsedge; Cyperus rotundus; Pasteur effect; weed ecology
5.  Influence of Environmental Factors, Cultural Practices, and Herbicide Application on Seed Germination and Emergence Ecology of Ischaemum rugosum Salisb 
PLoS ONE  2015;10(9):e0137256.
Ischaemum rugosum Salisb. (Saramolla grass) is a noxious weed of rice that is difficult to control by chemical or mechanical means once established. A study was conducted to determine the effect of light, temperature, salt, drought, flooding, rice residue mulch, burial depth, and pre-emergence herbicides on seed germination and emergence of I. rugosum. Germination was stimulated by light and inhibited under complete darkness. Optimum temperature for germination was 30/20°C (97.5% germination). Germination reduced from 31 to 3.5% when the osmotic potential of the growing medium decreased from -0.1 to -0.6 MPa and no germination occurred at -0.8 MPa. Germination was 18 and 0.5% at 50 and 100 mM NaCl concentrations, respectively, but was completely inhibited at 150 mM or higher. Residue application at 1–6 t ha-1 reduced weed emergence by 35–88% and shoot biomass by 55–95%. The efficacy of pre-emergence herbicides increased with increasing application rates and decreased with increasing rice residue mulching. The efficacy of herbicides was in the order of oxadiazon> pendimethalin> pretilachlor. At 6 t ha-1, all herbicides, regardless of rates, did not differ from the control treatment. I. rugosum seeds buried at 2 cm or deeper did not emerge; however, they emerged by 4.5 and 0.5% at 0.5 and 1 cm depths, respectively, compared to the 39% germination for soil surface seeding. Flooding at 4 DAS or earlier reduced seedling emergence and shoot biomass while flooding at 8 DAS reduced only seedling emergence. The depth and timing of flooding independently reduced root biomass. Flooding at 4 and 6 cm depths reduced the root biomass. Relative to flooding on the day of sowing, flooding at 8 DAS increased root biomass by 89%. Similarly, flooding on the day of sowing and at 2 DAS reduced the root–shoot biomass ratio. Under the no-flood treatment, increasing rates of pretilachlor from 0.075 to 0.3 kg ai ha-1 reduced weed emergence by 61–79%. At the flooding depth of 2–4 cm, pretilachlor reduced weed emergence and shoot and root biomass, but the differences across rates were non-significant. Information generated in this study will be helpful in developing integrated weed management strategies for managing this weed.
doi:10.1371/journal.pone.0137256
PMCID: PMC4569434  PMID: 26368808
6.  Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa) 
Annals of Botany  2008;103(2):197-209.
Background and Aims
Flooding slows seed germination, imposes fatalities and delays seedling establishment in direct-seeded rice. This study describes responses of contrasting rice genotypes subjected to flooding or low oxygen stress during germination and discusses the basis of tolerance shown by certain cultivars.
Methods
In one set of experiments, dry seeds were sown in soil and either watered normally or flooded with 10 cm of water. Seedling survival and shoot and root growth were assessed and seed portions of germinating seedlings were assayed for soluble sugars and starch concentrations. The whole germinating seedlings were assayed for amylase and peroxidase activities and for ethylene production. Activities of enzymes associated with anaerobic respiration were examined and gene expression was analysed separately with seeds germinating under different amounts of dissolved oxygen in dilute agar.
Key Results
Flooding during germination reduced survival but to a lesser extent in tolerant genotypes. Starch concentration in germinating seeds decreased while sugar concentration increased under flooding, but more so in tolerant genotypes. Amylase activity correlated positively with elongation (r = 0·85 for shoot and 0·83 for root length) and with plant survival (r = 0·92). Tolerant genotypes had higher amylase activity and higher RAmy3D gene expression. Ethylene was not detected in seeds within 2 d after sowing, but increased thereafter, with a greater increase in tolerant genotypes starting 3 d after sowing. Peroxidase activity was higher in germinating seeds of sensitive genotypes and correlated negatively with survival.
Conclusions
Under low oxygen stress, tolerant genotypes germinate, grow faster and more seedlings survive. They maintain their ability to use stored starch reserves through higher amylase activity and anaerobic respiration, have higher rates of ethylene production and lower peroxidase activity as germinating seeds and as seedlings. Relevance of these traits to tolerance of flooding during germination and early growth is discussed.
doi:10.1093/aob/mcn211
PMCID: PMC2707318  PMID: 19001425
Amylase; anoxia; crop establishment; direct-seeded rice; ethylene; flooding; germination; hypoxia; Oryza sativa
7.  Morphological and physiological responses of lowland purple nutsedge (Cyperus rotundus L.) to flooding 
AoB Plants  2010;2010:plq010.
Comparing a lowland and an upland ecotype of Cyperus rotundus, the former had greater carbohydrate reserves in tubers, thicker roots and stems with larger air spaces and, under hypoxia, it maintained relatively lower activities of alcohol dehydrogenase and lactate dehydrogenase.
Background and aims
Purple nutsedge (Cyperus rotundus L.) is a major weed of upland crops and vegetables. Recently, a flood-tolerant ecotype evolved as a serious weed in lowland rice. This study attempted to establish the putative growth and physiological features that led to this shift in adaptation.
Methodology
Tubers of upland C. rotundus (ULCR) and lowland C. rotundus (LLCR) ecotypes were collected from their native habitats and maintained under the respective growth conditions in a greenhouse. Five experiments were conducted to assess the variation between the two ecotypes in germination, growth and tuber morphology when grown in their native or ‘switched’ conditions. Carbohydrate storage and mobilization, and variation in anaerobic respiration under hypoxia were compared.
Principal results
Tubers of LLCR were larger than those of ULCR, with higher carbohydrate content, and larger tubers developed with increasing floodwater depth. Stems of LLCR had larger diameter and proportionally larger air spaces than those of ULCR: a method of aerating submerged plant parts. The LLCR ecotype can also mobilize and use carbohydrate reserves under hypoxia, and it maintained relatively lower and steadier activity of alcohol dehydrogenase (ADH) as a measure of sustained anaerobic respiration. In contrast, ADH activity in ULCR increased faster upon a shift to hypoxia and then sharply decreased, suggesting depletion of available soluble sugar substrates. The LLCR ecotype also maintained lower lactate dehydrogenase activity under flooded conditions, which could reduce chances of cellular acidosis.
Conclusions
These adaptive traits in the LLCR ecotype were expressed constitutively, but some of them, such as tuber growth and aerenchyma development, are enhanced with stress severity. The LLCR ecotype attained numerous adaptive traits that could have evolved as a consequence of natural evolution or repeated management practices, and alternative strategies are necessary because flooding is no longer a feasible management option.
doi:10.1093/aobpla/plq010
PMCID: PMC3000701  PMID: 22476068
8.  Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.) 
Rice is semi-aquatic, adapted to a wide range of hydrologies, from aerobic soils in uplands to anaerobic and flooded fields in waterlogged lowlands, to even deeply submerged soils in flood-prone areas. Considerable diversity is present in native rice landraces selected by farmers over centuries. Our understanding of the adaptive features of these landraces to native ecosystems has improved considerably over the recent past. In some cases, major genes associated with tolerance have been cloned, such as SUB1A that confers tolerance of complete submergence and SNORKEL genes that control plant elongation to escape deepwater. Modern rice varieties are sensitive to flooding during germination and early growth, a problem commonly encountered in rainfed areas, but few landraces capable of germination under these conditions have recently been identified, enabling research into tolerance mechanisms. Major QTLs were also identified, and are being targeted for molecular breeding and for cloning. Nevertheless, limited progress has been made in identifying regulatory processes for traits that are unique to tolerant genotypes, including faster germination and coleoptile elongation, formation of roots and leaves under hypoxia, ability to catabolize starch into simple sugars for subsequent use in glycolysis and fermentative pathways to generate energy. Here we discuss the state of knowledge on the role of the PDC-ALDH-ACS bypass and the ALDH enzyme as the likely candidates effective in tolerant rice genotypes. Potential involvement of factors such as cytoplasmic pH regulation, phytohormones, reactive oxygen species scavenging and other metabolites is also discussed. Further characterization of contrasting genotypes would help in elucidating the genetic and biochemical regulatory and signaling mechanisms associated with tolerance. This could facilitate breeding rice varieties suitable for direct seeding systems and guide efforts for improving waterlogging tolerance in other crops.
doi:10.3389/fpls.2013.00269
PMCID: PMC3719019  PMID: 23888162
anaerobic germination; alcoholic fermentation; ALDH; pyruvate dehydrogenase bypass; hypoxia; direct seeding; flooding; submergence tolerance
9.  Physiological and Morphological Responses of Ischaemum rugosum Salisb. (Wrinkled Grass) to Different Nitrogen Rates and Rice Seeding Rates 
PLoS ONE  2014;9(6):e98255.
Ischaemum rugosum is a competitive weed in direct-seeded rice systems. Developing integrated weed management strategies that promote the suppression of weeds by crop density, cultivar selection, and nutrition requires better understanding of the extent to which rice interferes with the growth of this weed and how it responds to resource limitation due to rice interference. The growth of I. rugosum was studied when grown with four rice seeding rates (0, 25, 50, and 100 kg ha−1) and four nitrogen (N) rates (0, 50, 100, and 150 kg ha−1). Compared to the weed plants grown alone, weed tiller number was reduced by 63–80%, leaf number by 68–77%, leaf area by 69–77%, leaf biomass by 72–84%, and inflorescence biomass by 81–93% at the rice seeding rates of 25–100 kg ha−1. All these parameters increased with increasing rates of N from 0 to 150 kg ha−1. At weed maturity, I. rugosum plants were 100% taller than rice at 0 kg N ha−1, whereas, with added N, the weeds were only 50% taller than rice. Weed biomass increased by 82–160%, whereas rice biomass increased by 92–229%, with the application of 50–150 kg N ha−1. Added N favored rice biomass production more than it did the weed. Rice interference reduced the height and biomass of I. rugosum, but did not suppress its growth completely. I. rugosum showed the ability to reduce the effects of rice interference by increasing leaf area, leaf weight ratio, and specific leaf area, and by decreasing the root-shoot weight ratio in comparison to the weed plants grown alone. The results suggest that rice crop interference alone may reduce I. rugosum growth but may not provide complete control of this weed. The need for integrated weed management practices to effectively control this weed species is highlighted.
doi:10.1371/journal.pone.0098255
PMCID: PMC4049584  PMID: 24910995
10.  Seed germination and seedling development in response to submergence in tree species of the Central Amazonian floodplains 
AoB Plants  2015;7:plv041.
This study shows that Central Amazonian floodplain trees can cope with long-term flooding during the early life-history stages. Seven of the eight studied species germinated and formed seedlings under water that endured submersion without any apparent injury for periods of 20 to 115 days, depending on the species. Only one of the seven did not survive re-exposure to air. The ability to germinate and form seedlings in water that subsequently are able to thrive in aerated soils would allow the most use of the short terrestrial phase available for seedling establishment in the lower portions of the flood-level gradient.
Successful germination and seedling establishment are crucial steps for maintenance and expansion of plant populations and recovery from perturbations. Every year the Amazon River and its tributaries overflow and flood the adjacent forest, exerting a strong selective pressure on traits related to seedling recruitment. We examined seed characteristics, stored reserves, germination, seedling development and survival under water of eight representative tree species from the lower portions of the flood-level gradient to identify adaptive strategies that contribute to their regeneration in this extreme ecosystem. Submerged seedlings were assessed for longevity and survival until they showed symptoms of injury. At this point, the remaining healthy seedlings were planted in unsaturated soil to monitor recovery after re-exposure to air over 30 days. All small (seed mass ≤0.17 g) seeds had epigeal phanerocotylar-type germination, a trait that would allow plants to acquire light and CO2 in the shortest time. Cell wall storage polysaccharide was a major component of all seeds, suggesting plant investment in structural reserves. Seven of the eight species germinated and formed healthy seedlings under water that endured submersion without any apparent injury for periods of 20–115 days, depending on the species. Seedlings of some species changed the direction of root growth and grew towards the surface of the water, which might have increased the uptake of oxygen to the tissues. Only one of the seven species did not survive re-exposure to air. Species able to germinate and produce seedlings under submersion, which subsequently are able to establish in aerated soils, would have more time available for terrestrial growth. This is critical for colonization of lower portions of the flood-level gradient where establishment is constrained by the short terrestrial phase that precedes the next flood.
doi:10.1093/aobpla/plv041
PMCID: PMC4480040  PMID: 25922297
Carbohydrate reserves; cell wall storage polysaccharides; flood tolerance; seed germination in water; submergence tolerance; tropism
11.  Dynamics of Weeds in the Soil Seed Bank: A Hidden Markov Model to Estimate Life History Traits from Standing Plant Time Series 
PLoS ONE  2015;10(10):e0139278.
Predicting the population dynamics of annual plants is a challenge due to their hidden seed banks in the field. However, such predictions are highly valuable for determining management strategies, specifically in agricultural landscapes. In agroecosystems, most weed seeds survive during unfavourable seasons and persist for several years in the seed bank. This causes difficulties in making accurate predictions of weed population dynamics and life history traits (LHT). Consequently, it is very difficult to identify management strategies that limit both weed populations and species diversity. In this article, we present a method of assessing weed population dynamics from both standing plant time series data and an unknown seed bank. We use a Hidden Markov Model (HMM) to obtain estimates of over 3,080 botanical records for three major LHT: seed survival in the soil, plant establishment (including post-emergence mortality), and seed production of 18 common weed species. Maximum likelihood and Bayesian approaches were complementarily used to estimate LHT values. The results showed that the LHT provided by the HMM enabled fairly accurate estimates of weed populations in different crops. There was a positive correlation between estimated germination rates and an index of the specialisation to the crop type (IndVal). The relationships between estimated LHTs and that between the estimated LHTs and the ecological characteristics of weeds provided insights into weed strategies. For example, a common strategy to cope with agricultural practices in several weeds was to produce less seeds and increase germination rates. This knowledge, especially of LHT for each type of crop, should provide valuable information for developing sustainable weed management strategies.
doi:10.1371/journal.pone.0139278
PMCID: PMC4591344  PMID: 26427023
12.  Analysis of Stress-Responsive Gene Expression in Cultivated and Weedy Rice Differing in Cold Stress Tolerance 
PLoS ONE  2015;10(7):e0132100.
Rice (Oryza sativa L.) cultivars show impairment of growth in response to environmental stresses such as cold at the early seedling stage. Locally adapted weedy rice is able to survive under adverse environmental conditions, and can emerge in fields from greater soil depth. Cold-tolerant weedy rice can be a good genetic source for developing cold-tolerant, weed-competitive rice cultivars. An in-depth analysis is presented here of diverse indica and japonica rice genotypes, mostly weedy rice, for cold stress response to provide an understanding of different stress adaptive mechanisms towards improvement of the rice crop performance in the field. We have tested a collection of weedy rice genotypes to: 1) classify the subspecies (ssp.) grouping (japonica or indica) of 21 accessions; 2) evaluate their sensitivity to cold stress; and 3) analyze the expression of stress-responsive genes under cold stress and a combination of cold and depth stress. Seeds were germinated at 25°C at 1.5- and 10-cm sowing depth for 10d. Seedlings were then exposed to cold stress at 10°C for 6, 24 and 96h, and the expression of cold-, anoxia-, and submergence-inducible genes was analyzed. Control plants were seeded at 1.5cm depth and kept at 25°C. The analysis revealed that cold stress signaling in indica genotypes is more complex than that of japonica as it operates via both the CBF-dependent and CBF-independent pathways, implicated through induction of transcription factors including OsNAC2, OsMYB46 and OsF-BOX28. When plants were exposed to cold + sowing depth stress, a complex signaling network was induced that involved cross talk between stresses mediated by CBF-dependent and CBF-independent pathways to circumvent the detrimental effects of stresses. The experiments revealed the importance of the CBF regulon for tolerance to both stresses in japonica and indica ssp. The mechanisms for cold tolerance differed among weedy indica genotypes and also between weedy indica and cultivated japonica ssp. as indicated by the up/downregulation of various stress-responsive pathways identified from gene expression analysis. The cold-stress response is described in relation to the stress signaling pathways, showing complex adaptive mechanisms in different genotypes.
doi:10.1371/journal.pone.0132100
PMCID: PMC4521806  PMID: 26230579
13.  Learning from nature: the use of non-model species to identify novel acclimations to flooding stress 
AoB Plants  2014;6:plu016.
Floods have a severe impact on plant performance. In general, crops are flood intolerant and are at an increased risk to flooding events due to global climate change. It is a grand challenge to improve agricultural production to feed the increasing human world population despite the increase of flooding stress. Mechanistic understanding of flooding tolerance is mainly achieved with model species such as Oryza sativa and Arabidopsis thaliana. However, wild plants from flood-prone environments have evolved in frequently flooded environments and therefore possess unique traits that facilitate growth and reproduction during and after flooding stress. Flooding research with these non-model wild plants might help us to identify novel adaptive traits that can be applied to improve flooding tolerance of crops.
Excess water in the form of waterlogged soil or deeper submergence (generically termed ‘flooding’) influences plant growth, survival and species distribution in many natural ecosystems. It also has a negative impact on crop growth and yield since many agricultural species are flooding intolerant. The often devastating effect of flooding on plant performance is related to its interference with gas exchange between the plant and its environment. This results in energy deficiency and carbohydrate starvation. In the near future, flooding frequency is expected to increase due to global climate change and the human population is expected to increase to ∼9 billion people by 2050. The need for increased agricultural productivity is self-evident and this will require a better mechanistic understanding of the interaction between plants and abiotic stresses such as flooding. We argue that, in seeking this understanding, we should not restrict the research to model species such as rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana). This is because some stress-tolerance mechanisms are not found in these species. Examples are given of how flooding tolerance is achieved by non-model species of Rumex and Rorippa that have evolved to cope with flooding in natural environments. These findings will add usefully to the spread of resources available to plant breeding programmes aimed at improving flooding tolerance in crop plants.
doi:10.1093/aobpla/plu016
PMCID: PMC4011469  PMID: 24876298
Abscisic acid; climate change; ethylene; flooding; learning from nature; Rorippa; Rumex; waterlogging.
14.  Ozone Exposure of a Weed Community Produces Adaptive Changes in Seed Populations of Spergula arvensis 
PLoS ONE  2013;8(9):e75820.
Tropospheric ozone is one of the major drivers of global change. This stress factor alters plant growth and development. Ozone could act as a selection pressure on species communities composition, but also on population genetic background, thus affecting life history traits. Our objective was to evaluate the consequences of prolonged ozone exposure of a weed community on phenotypic traits of Spergulaarvensis linked to persistence. Specifically, we predicted that the selection pressure exerted by high ozone concentrations as well as the concomitant changes in the weed community would drive population adaptive changes which will be reflected on seed germination, dormancy and longevity. In order to test seed viability and dormancy level, we conducted germination experiments for which we used seeds produced by S. arvensis plants grown within a weed community exposed to three ozone treatments during four years (0, 90 and 120 ppb). We also performed a soil seed bank experiment to test seed longevity with seeds coming from both the four-year ozone exposure experiment and from a short-term treatment conducted at ambient and added ozone concentrations. We found that prolonged ozone exposure produced changes in seed germination, dormancy and longevity, resulting in three S. arvensis populations. Seeds from the 90 ppb ozone selection treatment had the highest level of germination when stored at 75% RH and 25 °C and then scarified. These seeds showed the lowest dormancy level when being subjected to 5 ºC/5% RH and 25 ºC/75% followed by 5% RH storage conditions. Furthermore, ozone exposure increased seed persistence in the soil through a maternal effect. Given that tropospheric ozone is an important pollutant in rural areas, changes in seed traits due to ozone exposure could increase weed persistence in fields, thus affecting weed-crop interactions, which could ultimately reduce crop production.
doi:10.1371/journal.pone.0075820
PMCID: PMC3784398  PMID: 24086640
15.  Direct and reverse pollen-mediated gene flow between GM rice and red rice weed 
AoB Plants  2013;5:plt050.
Several studies have reported transgenic rice transferring transgenes to red rice weed. However, gene flow also occurs in the opposite direction resulting in transgenic seeds that have incorporated the traits of wild red rice. We quantified this reverse flow being higher than the direct gene flow, nevertheless transgenic seeds carrying wild genes would remain in the spike and therefore most of it would be removed at harvesting. This phenomenon must be considered in fields used for elite seed production and in developing countries where there is a higher risk of GM red rice weed infestation increasing from year to year.
Potential risks of genetically modified (GM) crops must be identified before their commercialization, as happens with all new technologies. One of the major concerns is the proper risk assessment of adventitious presence of transgenic material in rice fields due to cross-pollination. Several studies have been conducted in order to quantify pollen-mediated gene flow from transgenic rice (Oryza sativa) to both conventional rice and red rice weed (O. sativa f. spontanea) under field conditions. Some of these studies reported GM pollen-donor rice transferring GM traits to red rice. However, gene flow also occurs in the opposite direction, in a phenomenon that we have called reverse gene flow, resulting in transgenic seeds that have incorporated the traits of wild red rice. We quantified reverse gene flow using material from two field trials. A molecular analysis based on amplified fragment length polymorphisms was carried out, being complemented with a phenotypic identification of red rice traits. In both field trials, the reverse gene flow detected was greater than the direct gene flow. The rate of direct gene flow varied according to the relative proportions of the donor (GM rice) and receptor (red rice) plants and was influenced by wind direction. The ecological impact of reverse gene flow is limited in comparison with that of direct gene flow because non-shattered and non-dormant seeds would be obtained in the first generation. Hybrid seed would remain in the spike and therefore most of it would be removed during harvesting. Nevertheless, this phenomenon must be considered in fields used for elite seed production and in developing countries where farmers often keep some seed for planting the following year. In these cases, there is a higher risk of GM red rice weed infestation increasing from year to year and therefore a proper monitoring plan needs to be established.
doi:10.1093/aobpla/plt050
PMCID: PMC4130427
Field trial; gene flow; herbicide resistance; Oryza sativa; red rice; risk assessment; transgenic rice.
16.  Response of Rice Genotypes to Weed Competition in Dry Direct-Seeded Rice in India 
The Scientific World Journal  2014;2014:641589.
The differential weed-competitive abilities of eight rice genotypes and the traits that may confer such attributes were investigated under partial weedy and weed-free conditions in naturally occurring weed flora in dry direct-seeded rice during the rainy seasons of 2011 and 2012 at Ludhiana, Punjab, India. The results showed genotypic differences in competitiveness against weeds. In weed-free plots, grain yield varied from 6.6 to 8.9 t ha−1 across different genotypes; it was lowest for PR-115 and highest for the hybrid H-97158. In partial weedy plots, grain yield and weed biomass at flowering varied from 3.6 to 6.7 t ha−1 and from 174 to 419 g m−2, respectively. In partial weedy plots, grain yield was lowest for PR-115 and highest for PR-120. Average yield loss due to weed competition ranged from 21 to 46% in different rice genotypes. The study showed that early canopy closure, high leaf area index at early stage, and high root biomass and volume correlated positively with competitiveness. This study suggests that some traits (root biomass, leaf area index, and shoot biomass at the early stage) could play an important role in conferring weed competitiveness and these traits can be explored for dry-seeded rice.
doi:10.1155/2014/641589
PMCID: PMC4100294  PMID: 25093205
17.  Seed Germination Ecology of Feather Lovegrass [Eragrostis tenella (L.) Beauv. Ex Roemer & J.A. Schultes] 
PLoS ONE  2013;8(11):e79398.
Feather lovegrass [Eragrostis tenella (L.) Beauv. Ex Roemer & J.A. Schultes] is a C4 grass weed that has the ability to grow in both lowland and upland conditions. Experiments were conducted in the laboratory and screenhouse to evaluate the effect of environmental factors on germination, emergence, and growth of this weed species. Germination in the light/dark regime was higher at alternating day/night temperatures of 30/20 °C (98%) than at 35/25 °C (83%) or 25/15 °C (62%). Germination was completely inhibited by darkness. The osmotic potential and sodium chloride concentrations required for 50% inhibition of maximum germination were -0.7 MPa and 76 mM, respectively. The highest seedling emergence (69%) was observed from the seeds sown on the soil surface and no seedlings emerged from seeds buried at depths of 0.5 cm or more. The use of residue as mulches significantly reduced the emergence and biomass of feather lovegrass seedlings. A residue amount of 0.5 t ha-1 was needed to suppress 50% of the maximum seedlings. Because germination was strongly stimulated by light and seedling emergence was the highest for the seeds sown on the soil surface, feather lovegrass is likely to become a problematic weed in zero-till systems. The knowledge gained from this study could help in developing effective and sustainable weed management strategies.
doi:10.1371/journal.pone.0079398
PMCID: PMC3821846  PMID: 24255700
18.  The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions 
Annals of Botany  2009;104(6):1111-1119.
Background and Aims
In the Amazonian floodplains plants withstand annual periods of flooding which can last 7 months. Under these conditions seedlings remain submerged in the dark for long periods since light penetration in the water is limited. Himatanthus sucuuba is a tree species found in the ‘várzea’ (VZ) floodplains and adjacent non-flooded ‘terra-firme’ (TF) forests. Biochemical traits which enhance flood tolerance and colonization success of H. sucuuba in periodically flooded environments were investigated.
Methods
Storage carbohydrates of seeds of VZ and TF populations were extracted and analysed by HPAEC/PAD. Starch was analysed by enzyme (glucoamylase) degradation followed by quantification of glucose oxidase. Carbohydrate composition of roots of VZ and TF seedlings was studied after experimental exposure to a 15-d period of submersion in light versus darkness.
Key Results
The endosperm contains a large proportion of the seed reserves, raffinose being the main non-structural carbohydrate. Around 93 % of the cell wall storage polysaccharides (percentage dry weight basis) in the endosperm of VZ seeds was composed of mannose, while soluble sugars accounted for 2·5%. In contrast, 74 % of the endosperm in TF seeds was composed of galactomannans, while 22 % of the endosperm was soluble sugars. This suggested a larger carbohydrate allocation to germination in TF populations whereas VZ populations allocate comparatively more to carbohydrates mobilized during seedling development. The concentration of root non-structural carbohydrates in non-flooded seedlings strongly decreased after a 15-d period of darkness, whereas flooded seedlings were less affected. These effects were more pronounced in TF seedlings, which showed significantly lower root non-structural carbohydrate concentrations.
Conclusions
There seem to be metabolic adjustments in VZ but not TF seedlings that lead to adaptation to the combined stresses of darkness and flooding. This seems to be important for the survival of the species in these contrasting environments, leading these populations to different directions during evolution.
doi:10.1093/aob/mcp212
PMCID: PMC2766203  PMID: 19770164
Carbohydrate reserves; Himatanthus sucuuba; submergence tolerance; floodplains; galactomannans; raffinose; population differentiation; Amazon; storage
19.  Expression of Tolerance for Meloidogyne graminicola in Rice Cultivars as Affected by Soil Type and Flooding 
Journal of Nematology  2000;32(3):309-317.
The effects of different water regimes on the pathogenicity of Meloidogyne graminicola on six rice cultivars were determined in two soil types in three greenhouse experiments. Two water regimes, simulating continuous flooding and intermittent flooding, were used with five of the cultivars. All cultivars were susceptible to the nematode, but IR72 and IR74 were more tolerant than IR20 and IR29 under intermittent flooding. All were tolerant under continuous flooding. UPLRi-5 was grown under multiple water regimes: no flooding; continuous flooding; flooding starting at maximum tillering, panicle initiation, or booting stage; and flooding from sowing until maximum tillering or booting. In sandy loam soil, M. graminicola reduced stem and leaf dry weight, root dry weight, and grain weight under all water regimes. In clay loam soil, the nematode reduced root weight when the soil was not flooded or flooded only for a short time, from panicle initiation, or booting to maturity, and from sowing to maximum tillering. In clay loam soil, stem and leaf dry weight, as well as grain weight, were reduced by the nematode under all water regimes except continuous flooding or when the soil was flooded from sowing to booting stage. These results indicate that rice cultivar tolerance of M. graminicola varies with water regime and that yield losses due to M. graminicola may be prevented or minimized when the rice crop is flooded early and kept flooded until a late stage of development.
PMCID: PMC2620461  PMID: 19270982
Meloidogyne graminicola; pathogenicity; rice; tolerance; water regime
20.  Flooding tolerance in interspecific introgression lines containing chromosome segments from teosinte (Zea nicaraguensis) in maize (Zea mays subsp. mays) 
Annals of Botany  2013;112(6):1125-1139.
Background and Aims
Nicaraguan teosinte (Zea nicaraguensis), a species found in frequently flooded areas, provides useful germplasm for breeding flooding-tolerant maize (Z. mays subsp. mays). The objective of this study was to select flooding-tolerant lines using a library of introgression lines (ILs), each containing a chromosome segment from Z. nicaraguensis in the maize inbred line Mi29.
Methods
To produce the ILs, a single F1 plant derived from a cross between maize Mi29 and Z. nicaraguensis was backcrossed to Mi29 three times, self-pollinated four times and genotyped using simple sequence repeat markers. Flooding tolerance was evaluated at the seedling stage under reducing soil conditions.
Key Results
By backcrossing and selfing, a series of 45 ILs were developed covering nearly the entire maize genome. Five flooding-tolerant lines were identified from among the ILs by evaluating leaf injury. Among these, line IL#18, containing a Z. nicaraguensis chromosome segment on the long arm of chromosome 4, showed the greatest tolerance to flooding, suggesting the presence of a major quantitative trait locus (QTL) in that region. The presence of the QTL was verified by examining flooding tolerance in a population segregating for the candidate region of chromosome 4. There was no significant relationship between the capacity to form constitutive aerenchyma and flooding tolerance in the ILs, indicating the presence of other factors related to flooding tolerance under reducing soil conditions.
Conclusions
A flooding-tolerant genotype, IL#18, was identified; this genotype should be useful for maize breeding. In addition, because the chromosome segments of Z. nicaraguensis in the ILs cover nearly the entire genome and Z. nicaraguensis possesses several unique traits related to flooding tolerance, the ILs should be valuable material for additional QTL detection and the development of flooding-tolerant maize lines.
doi:10.1093/aob/mct160
PMCID: PMC3783227  PMID: 23877074
Aerenchyma; flooding tolerance; genetic resources; introgression lines; quantitative trait loci; QTL; recombination suppression; reducing soil conditions; teosinte; waterlogging; wide hybridization
21.  Conditions Leading to High CO2 (>5 kPa) in Waterlogged–Flooded Soils and Possible Effects on Root Growth and Metabolism 
Annals of Botany  2006;98(1):9-32.
• Aims Soil waterlogging impedes gas exchange with the atmosphere, resulting in low PO2 and often high PCO2. Conditions conducive to development of high PCO2 (5–70 kPa) during soil waterlogging and flooding are discussed. The scant information on responses of roots to high PCO2 in terms of growth and metabolism is reviewed.
• Scope PCO2 at 15–70 kPa has been reported for flooded paddy-field soils; however, even 15 kPa PCO2 may not always be reached, e.g. when soil pH is above 7. Increases of PCO2 in soils following waterlogging will develop much more slowly than decreases in PO2; in soil from rice paddies in pots without plants, maxima in PCO2 were reached after 2–3 weeks. There are no reliable data on PCO2 in roots when in waterlogged or flooded soils. In rhizomes and internodes, PCO2 sometimes reached 10 kPa, inferring even higher partial pressures in the roots, as a CO2 diffusion gradient will exist from the roots to the rhizomes and shoots. Preliminary modelling predicts that when PCO2 is higher in a soil than in roots, PCO2 in the roots would remain well below the PCO2 in the soil, particularly when there is ventilation via a well-developed gas-space continuum from the roots to the atmosphere. The few available results on the effects of PCO2 at > 5 kPa on growth have nearly all involved sudden increases to 10–100 kPa PCO2; consequently, the results cannot be extrapolated with certainty to the much more gradual increases of PCO2 in waterlogged soils. Nevertheless, rice in an anaerobic nutrient solution was tolerant to 50 kPa CO2 being suddenly imposed. By contrast, PCO2 at 25 kPa retarded germination of some maize genotypes by 50 %. With regard to metabolism, assuming that the usual pH of the cytoplasm of 7·5 was maintained, every increase of 10 kPa CO2 would result in an increase of 75–90 mm HCO3− in the cytoplasm. pH maintenance would depend on the biochemical and biophysical pH stats (i.e. regulatory systems). Furthermore, there are indications that metabolism is adversely affected when HCO3− in the cytoplasm rises above 50 mm, or even lower; succinic dehydrogenase and cytochrome oxidase are inhibited by HCO3− as low as 10 mm. Such effects could be mitigated by a decrease in the set point for the pH of the cytoplasm, thus lowering levels of HCO3− at the prevailing PCO2 in the roots.
• Conclusions Measurements are needed on PCO2 in a range of soil types and in roots of diverse species, during waterlogging and flooding. Species well adapted to high PCO2 in the root zone, such as rice and other wetland plants, thrive even when PCO2 is well over 10 kPa; mechanisms of adaptation, or acclimatization, by these species need exploration.
doi:10.1093/aob/mcl076
PMCID: PMC3291891  PMID: 16644893
Acid load; aerenchyma; bicarbonate; carbon dioxide; cytochrome c; O2 deficiency; pH regulation; metabolism; respiration; waterlogging; wetland plants
22.  Modelling Seedling Growth Rates of 18 Temperate Arable Weed Species as a Function of the Environment and Plant Traits 
Annals of Botany  2004;93(6):681-689.
• Background and Aims The early growth rate of seedlings in the exponential phase is an important eco‐ physiological trait in crop/weed competition models based on assessments of relative weed green area. An understanding of the role of various plant traits in determining early growth rate may also be useful for identifying contrasting weed strategies for establishment before canopy closure.
• Methods The response of seedling relative growth rate (RGR) to the environment was measured in outdoor sand beds in the autumn and the spring for 18 temperate annual weed species and two crops. Seedling growth was modelled using thermal time and effective day‐degrees (combining the effect of temperature and radiation). The contribution of various plant traits in determining variability in RGR was investigated using regression analysis.
• Key Results The effective day‐degree model was more effective for describing early weed growth than thermal time. Variability in RGR measured in the autumn was largely determined by differences between the species in net assimilation rate (NAR), whereas in the spring leaf area ratio (LAR) played a larger part. There were differences between the broadleaf and grass species in the relative contribution of NAR and LAR to RGR in both seasons. RGR in the spring was negatively correlated with initial seedling size.
• Conclusions The parameters derived in this study can be used to calibrate empirical models of crop yield loss based on relative weed green area to different growing seasons and assessment dates. The grass weeds, which tended to have large seeds, had a higher investment in roots in the seedling stage, potentially making them more competitive later in the season when resources become limiting.
doi:10.1093/aob/mch095
PMCID: PMC4242300  PMID: 15072977
Competition models; relative growth rate; broadleaf weeds; grass weeds
23.  The Mitochondrion-Located Protein OsB12D1 Enhances Flooding Tolerance during Seed Germination and Early Seedling Growth in Rice 
B12D belongs to a function unknown subgroup of the Balem (Barley aleurone and embryo) proteins. In our previous work on rice seed germination, we identified a B12D-like protein encoded by LOC_Os7g41350 (named OsB12D1). OsB12D1 pertains to an ancient protein family with an amino acid sequence highly conserved from moss to angiosperms. Among the six OsB12Ds, OsB12D1 is one of the major transcripts and is primarily expressed in germinating seed and root. Bioinformatics analyses indicated that OsB12D1 is an anoxic or submergence resistance-related gene. RT-PCR results showed OsB12D1 is induced remarkably in the coleoptiles or roots by flooding during seed germination and early seedling growth. The OsB12D1-overexpressed rice seeds could protrude radicles in 8 cm deep water, further exhibiting significant flooding tolerance compared to the wild type. Moreover, this tolerance was not affected by the gibberellin biosynthesis inhibitor paclobutrazol. OsB12D1 was identified in the mitochondrion by subcellular localization analysis and possibly enhances electron transport through mediating Fe and oxygen availability under flooded conditions. This work indicated that OsB12D1 is a promising gene that can help to enhance rice seedling establishment in farming practices, especially for direct seeding.
doi:10.3390/ijms150813461
PMCID: PMC4159805  PMID: 25089878
OsB12D1; flooding tolerance; mitochondrion; rice
24.  Integration of Agronomic Practices with Herbicides for Sustainable Weed Management in Aerobic Rice 
The Scientific World Journal  2013;2013:916408.
Till now, herbicide seems to be a cost effective tool from an agronomic view point to control weeds. But long term efficacy and sustainability issues are the driving forces behind the reconsideration of herbicide dependent weed management strategy in rice. This demands reappearance of physical and cultural management options combined with judicious herbicide application in a more comprehensive and integrated way. Keeping those in mind, some agronomic tools along with different manual weeding and herbicides combinations were evaluated for their weed control efficacy in rice under aerobic soil conditions. Combination of competitive variety, higher seeding rate, and seed priming resulted in more competitive cropping system in favor of rice, which was reflected in lower weed pressure, higher weed control efficiency, and better yield. Most of the herbicides exhibited excellent weed control efficiency. Treatments comprising only herbicides required less cost involvement but produced higher net benefit. On the contrary, treatments comprising both herbicide and manual weeding required high cost involvement and thus produced lower net benefit. Therefore, adoption of competitive rice variety, higher seed rate, and seed priming along with spraying different early-postemergence herbicides in rotation at 10 days after seeding (DAS) followed by a manual weeding at 30 DAS may be recommended from sustainability view point.
doi:10.1155/2013/916408
PMCID: PMC3808706  PMID: 24223513
25.  The biology of habitat dominance; can microbes behave as weeds? 
Microbial Biotechnology  2013;6(5):453-492.
Summary
Competition between microbial species is a product of, yet can lead to a reduction in, the microbial diversity of specific habitats. Microbial habitats can resemble ecological battlefields where microbial cells struggle to dominate and/or annihilate each other and we explore the hypothesis that (like plant weeds) some microbes are genetically hard-wired to behave in a vigorous and ecologically aggressive manner. These ‘microbial weeds’ are able to dominate the communities that develop in fertile but uncolonized – or at least partially vacant – habitats via traits enabling them to out-grow competitors; robust tolerances to habitat-relevant stress parameters and highly efficient energy-generation systems; avoidance of or resistance to viral infection, predation and grazers; potent antimicrobial systems; and exceptional abilities to sequester and store resources. In addition, those associated with nutritionally complex habitats are extraordinarily versatile in their utilization of diverse substrates. Weed species typically deploy multiple types of antimicrobial including toxins; volatile organic compounds that act as either hydrophobic or highly chaotropic stressors; biosurfactants; organic acids; and moderately chaotropic solutes that are produced in bulk quantities (e.g. acetone, ethanol). Whereas ability to dominate communities is habitat-specific we suggest that some microbial species are archetypal weeds including generalists such as: Pichia anomala, Acinetobacter spp. and Pseudomonas putida; specialists such as Dunaliella salina, Saccharomyces cerevisiae, Lactobacillus spp. and other lactic acid bacteria; freshwater autotrophs Gonyostomum semen and Microcystis aeruginosa; obligate anaerobes such as Clostridium acetobutylicum; facultative pathogens such as Rhodotorula mucilaginosa, Pantoea ananatis and Pseudomonas aeruginosa; and other extremotolerant and extremophilic microbes such as Aspergillus spp., Salinibacter ruber and Haloquadratum walsbyi. Some microbes, such as Escherichia coli, Mycobacterium smegmatis and Pseudoxylaria spp., exhibit characteristics of both weed and non-weed species. We propose that the concept of nonweeds represents a ‘dustbin’ group that includes species such as Synodropsis spp., Polypaecilum pisce, Metschnikowia orientalis, Salmonella spp., and Caulobacter crescentus. We show that microbial weeds are conceptually distinct from plant weeds, microbial copiotrophs, r-strategists, and other ecophysiological groups of microorganism. Microbial weed species are unlikely to emerge from stationary-phase or other types of closed communities; it is open habitats that select for weed phenotypes. Specific characteristics that are common to diverse types of open habitat are identified, and implications of weed biology and open-habitat ecology are discussed in the context of further studies needed in the fields of environmental and applied microbiology.
doi:10.1111/1751-7915.12027
PMCID: PMC3918151  PMID: 23336673

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