Photosynthetic acclimation is important for post-submergence recovery of photosynthesis and growth in two riparian species

Background and Aims

Concomitant increases in O₂ and irradiance upon de-submergence can cause photoinhibition and photo-oxidative damage to the photosynthetic apparatus of plants. As energy and carbohydrate supply from photosynthesis is needed for growth, it was hypothesized that post-submergence growth recovery may require efficient photosynthetic acclimation to increased O₂ and irradiance to minimize photo-oxidative damage. The hypothesis was tested in two flood-tolerant species: a C₃ herb, Alternanthera philoxeroides; and a C₄ grass, Hemarthria altissima. The impact of low O₂ and low light, typical conditions in turbid floodwater, on post-submergence recovery was assessed by different flooding treatments combined with shading.

Methods

Experiments were conducted during 30 d of flooding (waterlogging or submergence) with or without shading and subsequent recovery of 20 d under growth conditions. Changes in dry mass, number of branches/tillers, and length of the longest internodes and main stems were recorded to characterize growth responses. Photosynthetic parameters (photosystem II efficiency and non-photochemical quenching) were determined in mature leaves based on chlorophyll a fluorescence measurements.

Key Results

In both species growth and photosynthesis recovered after the end of the submergence treatment, with recovery of photosynthesis (starting shortly after de-submergence) preceding recovery of growth (pronounced on days 40–50). The effective quantum yield of photosystem II and non-photochemical quenching were diminished during submergence but rapidly increased upon de-submergence. Similar changes were found in all shaded plants, with or without flooding. Submerged plants did not suffer from photoinhibition throughout the recovery period although their growth recovery was retarded.

Conclusions

After sudden de-submergence the C₃ plant A. philoxeroides and the C₄ plant H. altissima were both able to maintain the functionality of the photosynthetic apparatus through rapid acclimation to changing O₂ and light conditions. The ability for photosynthetic acclimation may be essential for adaptation to wetland habitats in which water levels fluctuate.Key words: Aerenchyma, Alternanthera philoxeroides, flooding, growth, Hemarthria altissima, low light, photosynthesis, shade, submergence, waterlogging, wetland plant     

Morphological and physiological responses of rice seedlings to complete submergence (flash flooding)

Background and Aims

Reducing damage to rice seedlings caused by flash flooding will improve the productivity of rainfed lowland rice in West Africa. Accordingly, the morphological and physiological responses of different forms of rice to complete submergence were examined in field and pot experiments to identify primary causes of damage.

Methods

To characterize the physiological responses, seedlings from a wide genetic base including Oryza sativa, O. glaberrima and interspecific hybrids were compared using principle component analysis.

Key Results

Important factors linked to flash-flood tolerance included minimal shoot elongation underwater, increase in dry matter weight during submergence and post-submergence resistance to lodging. In particular, fast shoot elongation during submergence negatively affected plant growth after de-submergence. Also shoot-elongating cultivars showed a strong negative correlation between dry matter weight of the leaves that developed before submergence and leaves developing during submergence.

Conclusions

Enhancement of shoot elongation during submergence in water that is too deep to permit re-emergence by small seedlings represents a futile escape strategy that takes place at the expense of existing dry matter in circumstances where underwater photosynthetic carbon fixation is negligible. Consequently, it compromises survival or recovery growth once flood water levels recede and plants are re-exposed to the aerial environment. Tolerance is greater in cultivars where acceleration of elongation caused by submergence is minimal.Key words: Africa, flash floods, Oryza glaberrima, rainfed lowland, rice, shoot elongation, stress tolerance, submergence     

Morphological and anatomical changes of Melaleuca cajuputi under submergence

Melaleuca cajuputi is a woody plant of the Myrtaceae which is a dominant species in tropical peat swamps in southern Thailand, where the groundwater level fluctuates greatly. Although the current year seedlings are likely submerged, their adaptive responses have never been studied. The objective of the present study was to examine their responses to submergence, and especially their morphological and anatomical changes. Not only did the seedlings of M. cajuputi survive submergence for 56 days, but they could also increase their dry weight, shoot length, and leaf number during submergence. These growth responses to submergence indicate that the seedlings of M. cajuputi could make photosynthetic production under water. The leaves that developed under water were heterophyllous “aquatic leaves” that appear to represent adaptations to improve the uptake of gases from the water. Intercellular spaces in the stems and leaves were more strongly developed in the submerged seedlings than in non-submerged seedlings with the shoot and leaves in the air. The intercellular spaces appear to be schizogenous aerenchyma that facilitates gas exchange. The growth responses and anatomical responses in stems and leaves to submergence, which were found in M. cajuputi, are commonly known in herbaceous plants with amphibious characteristics, but had not been reported in woody plants. And our results suggest that M. cajuputi adapts to submergence similarly to other amphibious plants, thereby ensuring continuing biomass production.     

Chlorophyll fluorescence parameters,CO2 photosynthetic rate and regeneration capacity as a result of complete submergence and subsequent re-emergence in rice (Oryza sativa L.)

Regeneration capacity of submerged rice (Oryza sativa) seedlings in terms of CO₂ photosynthetic rate, chlorophyll a fluorescence and chlorophyll and carbohydrate content were investigated in three Indica rice cultivars namely FR 13A, Kalaputia and IR 42 that differed in submergence tolerance. Twenty-one day old plants were completely submerged under water for 8 days. Subsequently, plants were kept under normal conditions with 5–10 cm of stagnant water above soil surface for a further period of 15 days. After complete submergence, all genotypes showed inhibition of CO₂ photosynthetic rate. Submergence treatment resulted in a significant reduction of Rubisco activity. Maximal photochemical efficiency (F_v/F_m) of PS II and area above the fluorescence curve between F_o and F_m decreased more under submergence especially in susceptible cultivar IR 42. When re-aerated, the plants recovered to various degrees. The carbohydrate content of plants was found to be significantly and positively associated with submergence tolerance and regeneration growth. The tolerant cultivar (FR 13A) could survive submergence apparently because it possessed 1.9–2.0 and 3.2–3.7-fold more non-structural carbohydrate content before and after submergence compared to the susceptible cultivar (IR 42) and it had a better capability to restore its photosynthetic capacity during post-submergence periods.     

Molecular Events Underlying Coordinated Hormone Action in Submergence Escape Response of Deepwater Rice

Recent studies revealed that some rice varieties adopt opposite strategies to overcome flooding stress. While certain varieties hold metabolism and stay stunted until floodwater recedes, deepwater rice varieties undergo rapid stem elongation and do not suffer drowning problems. Both varieties use the same signaling agents, the ethylene response factors, as key factors even though they display opposite submergence responses. In deepwater rice, ethylene response factor genes SNORKEL1 and SNORKEL2 are believed to play a major role in submergence escape by mediating ethylene signaling, which leads to rapid stem elongation. These genes connect hormone signaling cascades from ethylene to ABA and gibberellins (GAs). Submergence increases ethylene levels in the internodal space, ethylene upregulates an ABA inactivating enzyme gene, OsCYP707A5 or OsABA8ox1, and some GA metabolism genes such as OsGA20ox genes and OsGA3ox genes. As a result of gene regulation by ethylene, internodal ABA levels decrease while GA levels increase, finally upregulating growth-related genes like expansin genes (OsEXPs). Along with the ethylene signaling in submergence, it is necessary to consider an alternative signaling pathway induced by hypoxia. Taken together, study on the submergence responses of rice plants will lead to improvement of crop production and contribution to basic research on plant growth.     

Physiology and proteomics analyses reveal the response mechanisms of Rhizophora mucronata seedlings to prolonged complete submergence

• Mangrove seedlings are subject to natural tidal inundation, while occasional flooding may lead to complete submergence. Complete submergence reduces light availability and limits gas exchange, affecting several plant metabolic processes. The present study focuses on Rhizophora mucronata, a common mangrove species found along the coasts of Thailand and the Malay Peninsula.
• To reveal response mechanisms of R. mucronata seedlings to submergence, a physiological investigation coupled with proteomic analyses of leaf and root tissues was carried out in plants subjected to 20 days of control (drained) or submerged conditions.
• Submerged seedlings showed decreased photosynthetic activity, lower stomatal conductance, higher total antioxidant capacity in leaves and higher lipid peroxidation in roots than control plants. At the same time, tissue nutrient ion content displayed organ-specific responses. Proteome analysis revealed a significant change in 240 proteins in the leaves and 212 proteins in the roots. In leaves, most differentially accumulated proteins (DAPs) are associated with nucleic acids, stress response, protein transport, signal transduction, development and photosynthesis. In roots, most DAPs are associated with protein metabolic process, response to abiotic stimulus, nucleic acid metabolism and transport.
• Our study provides a comprehensive understanding of submergence responses in R. mucronata seedlings. The results suggest that submergence induced multifaceted stresses related to light limitation, oxidative stress and osmotic stress, but the responses are organ specific. The results revealed many candidate proteins which may be essential for survival of R. mucronata under prolonged submergence.

     

Genes/QTLs affecting flood tolerance in rice

The adaptation of deepwater rice to flooding is attributed to two mechanisms, submergence tolerance and plant elongation. Using a QTL mapping study with replicated phenotyping under two contrasting (water qualities) submergence treatments and AFLP markers, we were able to identify several genes/QTLs that control plant elongation and submergence tolerance in a recombinant inbred rice population. Our results indicate that segregation of rice plants in their responses to different flooding stress conditions is largely due to the differential expression of a few key elongation and submergence tolerance genes. The most important gene was QIne1 mapped near sd-1 on chromosome 1. The Jalmagna (the deepwater parent) allele at this locus had a very large effect on internal elongation and contributed significantly to submergence tolerance under flooding. The second locus was a major gene, sub1(t), mapped to chromosome 9, which contributed to submergence tolerance only. The third one was a QTL, QIne4, mapped to chromosome 4. The IR74 (non-elongating parent) allele at this locus had a large effect for internal elongation. An additional locus that interacted strongly with both QIne1 and QIne4 appeared near RG403 on chromosome 5, suggesting a complex epistatic relationship among the three loci. Several QTLs with relatively small effects on plant elongation and submergence tolerance were also identified. The genetic aspects of these flooding tolerance QTLs with respect to patterns of differential expression of elongation and submergence tolerance genes under flooding are discussed. Received: 13 December 1999 / Accepted: 14 March 2000<@head-com-p1a.lf>Communicated by G. Wenzel     

EFFECTS OF LONG-TERM SUBMERGENCE ON SURVIVAL AND RECOVERY GROWTH OF FOUR RIPARIAN PLANT SPECIES IN THREE GORGES RESERVOIR REGION, CHINA

 地瓜藤(Ficus tikoua)、荻(Triarrhena sacchariflora)、牛鞭草(Hemarthria altissima)和狗牙根(Cynodon dactylon)是三峡库区常见的岸生植物, 自然分布于河岸带不同垂直高程的地段。为了明确它们在成库后“三峡库区消落区”长期完全水淹条件下的存活和生长情况, 实验设置对照(不进行水淹, 常规供水管理)和完全水淹两个处理, 30、60、90、120、150和180 d 6个水淹时间水平, 研究了4种植物在完全水淹条件下的存活、生物量变化和恢复生长。结果发现: 1) 4种植物在完全水淹条件下的存活率与其在河岸带上的垂直分布高程密切相关。分布于距江面高程较高的河岸段的地瓜藤植株, 在全淹30 d后就全部死亡; 分布在中高程河岸段的荻在全淹150和180 d后全部死亡; 可以分布于低高程河岸段的牛鞭草和狗牙根, 淹没180 d后存活率分别为90%和100%。2)全淹抑制了荻、牛鞭草和狗牙根的生长, 总生物量增量显著低于对照植株。与水淹0 d相比, 全淹处理植株的地上部分生物量显著降低, 荻在全淹60和120 d后, 地下部分生物量显著降低, 但牛鞭草和狗牙根的地下部分生物量与水淹0 d水平相比无显著差异。3)水淹处理结束后, 存活的荻、牛鞭草和狗牙根植株都能很好地恢复生长。在恢复生长过程中, 全淹30、60和90 d后, 荻、牛鞭草和狗牙根植株的总分枝长相对生长速率与对照植株无显著差异, 全淹120、150和180 d后, 牛鞭草和狗牙根植株的总分枝长相对生长速率显著高于对照植株。全淹处理的荻、牛鞭草和狗牙根植株的总叶片数相对生长速率始终显著高于对照植株。遭受长期完全水淹后, 植株在有限的营养储备条件下, 快速产生叶片以迅速积聚光合产物可能是植物更为优化的恢复生长方式。     

水淹胁迫诱导喜旱莲子草茎发生类环割效应

在水淹环境中,喜旱莲子草水面上未受淹的茎段常表现出增粗膨大的现象。遭受水淹的植物被淹没的组织和器官会面临氧气缺乏和能量供应不足的问题。植物体内碳水化合物的运输需要消耗能量,当因水淹而使植株被部分淹没（即地下部分全部和地上部分的一部分被淹没）时,由于水淹缺氧导致能量供应不足,碳水化合物在植物被淹组织内的运输可能受限从而在水面上的未淹茎段中积累并对未淹茎段的径向形态产生影响。为探究水淹环境中喜旱莲子草未受淹茎段增粗膨大是否与碳水化合物积累有关,对茎被水淹和茎不受水淹的喜旱莲子草进行对比研究,结果发现：（1）水淹的喜旱莲子草位于水面上的未淹茎段节间平均直径显著大于水面下受淹茎段节间平均直径,未淹茎段与受淹茎段相比发生显著的膨大现象;未水淹的喜旱莲子草其茎的上部茎段节间平均直径与下部茎段节间平均直径相比并无显著差异,上部茎段也无明显膨大现象。（2）水淹的喜旱莲子草位于水面上的未淹茎段碳水化合物含量显著高于未水淹的喜旱莲子草对应茎段的碳水化合物含量。本研究表明,水淹胁迫下喜旱莲子草位于水面上的未受淹茎段中碳水化合物发生积累,导致植株位于水面上的未受淹茎段发生与物理环割后类似的茎膨大现象。     

De-submergence-induced ethylene production in Rumex palustris: regulation and ecophysiological significance

Rumex palustris responds to total submergence by increasing the elongation rate of young petioles. This favours survival by shortening the duration of submergence. Underwater elongation is stimulated by ethylene entrapped within the plant by surrounding water. However, abnormally fast extension rates were found to be maintained even when leaf tips emerged above the floodwater. This fast post-submergence growth was linked to a promotion of ethylene production that is presumed to compensate for losses brought about by ventilation. Three sources of ACC contributed to post-submergence ethylene production in R. palustris: (i) ACC that had accumulated in the roots during submergence and was transported in xylem sap to the shoot when stomata re-opened and transpiration resumed, (ii) ACC that had accumulated in the shoot during the preceding period of submergence and (iii) ACC produced de novo in the shoot following de-submergence. This new production of ethylene was associated with increased expression of an ACC synthase gene (RP-ACS1) and an ACC oxidase gene (RP-ACO1), increased ACC synthase activity and a doubling of ACC oxidase activity, measured in vitro. Out of seven species of Rumex examined, a de-submergence upsurge in ethylene production was seen only in shoots of those that had the ability to elongate fast when submerged.     

水体溶氧影响陆生植物喜旱莲子草(Alternanthera philoxeroides)和牛鞭草(Hemarthria altissima)对完全水淹的耐受力

溶氧是水环境中一个重要的环境因子,为了探讨水中的溶氧含量水平是否会对陆生植物的耐淹能力造成影响,研究了陆生植物喜旱莲子草(Alternanthera philoxeroides)和牛鞭草(Hemarthria altissima)在遭受不同溶氧含量水体完全淹没后的生长表现、存活情况和非结构碳水化合物的变化。实验结果表明:(1)水体中的溶氧含量显著影响了处于完全水淹环境中的喜旱莲子草和牛鞭草的存活。受高溶氧水体完全水淹的喜旱莲子草和牛鞭草主茎的完好程度和存活叶的数量均显著高于遭受低溶氧水体完全水淹的喜旱莲子草和牛鞭草,喜旱莲子草和牛鞭草在高溶氧水体完全水淹后的生物量比低溶氧水体完全水淹后要高;(2)水体中的溶氧含量显著影响了处于完全水淹环境中的喜旱莲子草和牛鞭草的生长,受高溶氧水体完全水淹的喜旱莲子草主茎伸长生长和不定根生长显著强于受低溶氧水体完全水淹的喜旱莲子草,在不定根的生长上牛鞭草也具有同样的表现。(3)高溶氧水环境有利于减小被完全淹没的喜旱莲子草和牛鞭草的碳水化合物消耗,两种植物在受高溶氧完全水淹后体内具有的非结构性碳水化合物含量均比受低溶氧完全水淹后高。(4)喜旱莲子草比牛鞭草能更好地耐受完全水淹,当处于低溶氧完全水淹时表现得更为明显,本研究表明入侵物种喜旱莲子草比本地物种牛鞭草具有更强的环境适应能力和水淹耐受能力。     

鄱阳湖洲滩湿地植物生长和营养繁殖对水淹时长的响应

水淹时长是影响湿地植物分布的重要因素。在水情不断变化的背景下,鄱阳湖洲滩湿地植物种群和群落的变化规律还不清楚。为了探究淹水时长对鄱阳湖洲滩3种优势植物生长和繁殖的影响,并预测在水文发生剧烈变化后,3种优势植物分布的趋势,采用控制实验模拟了不同水淹时长(0、60、90、120、150 d和180 d)下鄱阳湖湿地3种优势植物(灰化薹草(Carex cinerascens)、南荻(Miscanthus lutarioriparius)和虉草(Phalaris arundinacea))的生长和繁殖情况。研究结果表明:1)南荻在水淹超过120 d后,存活率开始降低,水淹到达180 d完全死亡。而灰化薹草和虉草在淹水180 d后仍全部存活。表明南荻耐淹水的能力弱于其他两种植物。2)水淹显著降低灰化薹草的总生物量,并且总生物量随水淹时长的增加而逐渐降低。而短时间(小于150 d)的水淹没有对虉草总生物量产生显著影响。3)退水初期,灰化薹草的恢复生长趋向于地上部分,而虉草表现为地下和地下部分同步生长。该研究结果可以为预测水文情势变化下鄱阳湖湿地植物种群和群落的动态变化提供依据。     

Growth responses and non-structural carbohydrates in three wetland macrophyte species following submergence and de-submergence

We investigated the responses of growth and non-structural carbohydrates to submergence and de-submergence in three wetland macrophyte species. Survival rate, recovery ability, and soluble sugar and starch contents of flood-tolerant Polygonum hydropiper and of flood-sensitive Phalaris arundinacea and Carex argyi from Dongting Lake wetlands were investigated after 20, 40, and 60 days of complete submergence without light and 10 days after de-submergence. Plant dry weight and soluble sugar and starch contents decreased in all species during the submergence period. The decreases were slowest in P. hydropiper, intermediate in C. argyi, and most rapid in P. arundinacea. After 60 days of submergence, survival rates were 100, 50, and 0 % in P. hydropiper, C. argyi, and P. arundinacea, respectively. After recovery, plant dry weight increased in P. hydropiper and in C. argyi, but decreased in P. arundinacea. Compared to pre-submergence, soluble sugar contents generally increased and then remained relatively constant after recovery in all species, while starch content increased in P. hydropiper and decreased in P. arundinacea with increasing submergence time. For C. argyi, starch content decreased after recovery from the 20-day submergence, but increased after recovery from the 40- and 60-day submergences. These data illustrate mechanisms behind the flood tolerance of P. hydropiper and the sensitivity to flooding in P. arundinacea and C. argyi. These mechanisms include lower consumption and quicker accumulation of non-structural carbohydrates in flood-tolerant plants.     

The key regulator of submergence tolerance,SUB1A,promotes photosynthetic and metabolic recovery from submergence damage in rice leaves

The submergence‐tolerance regulator, SUBMERGENCE1A (SUB1A), of rice (Oryza sativa L.) modulates gene regulation, metabolism and elongation growth during submergence. Its benefits continue during desubmergence through protection from reactive oxygen species and dehydration, but there is limited understanding of SUB1A's role in physiological recovery from the stress. Here, we investigated the contribution of SUB1A to desubmergence recovery using the two near‐isogenic lines, submergence‐sensitive M202 and tolerant M202(Sub1). No visible damage was detected in the two genotypes after 3 d of submergence, but the sublethal stress differentially altered photosynthetic parameters and accumulation of energy reserves. Submergence inhibited photosystem II photochemistry and stimulated breakdown of protein and accumulation of several amino acids in both genotypes at similar levels. Upon desubmergence, however, more rapid return to homeostasis of these factors was observed in M202(Sub1). Submergence considerably restrained non‐photochemical quenching (NPQ) in M202, whereas the value was unaltered in M202(Sub1) during the stress. Upon reaeration, submerged plants encounter sudden exposure to higher light. A greater capability for NPQ‐mediated photoprotection can benefit the rapid recovery of photosynthetic performance and energy reserve metabolism in M202(Sub1). Our findings illuminate the significant role of SUB1A in active physiological recovery upon desubmergence, a component of enhanced tolerance to submergence.     

Shoot atmospheric contact is of little importance to aeration of deeper portions of the wetland plant Meionectes brownii; submerged organs mainly acquire O2 from the water column or produce it endogenously in underwater photosynthesis

Partial shoot submergence is considered less stressful than complete submergence of plants, as aerial contact allows gas exchange with the atmosphere. In situ microelectrode studies of the wetland plant Meionectes brownii showed that O₂ dynamics in the submerged stems and aquatic roots of partially submerged plants were similar to those of completely submerged plants, with internal O₂ concentrations in both organs dropping to less than 5 kPa by dawn regardless of submergence level. The anatomy at the nodes and the relationship between tissue porosity and rates of O₂ diffusion through stems were studied. Stem internodes contained aerenchyma and had mean gas space area of 17.7% per cross section, whereas nodes had 8.2%, but nodal porosity was highly variable, some nodes had very low porosity or were completely occluded (ca. 23% of nodes sampled). The cumulative effect of these low porosity nodes would have impeded internal O₂ movement down stems. Therefore, regardless of the presence of an aerial connection, the deeper portions of submerged organs sourced most of their O₂ via inwards diffusion from the water column during the night, and endogenous production in underwater photosynthesis during the daytime.     

漓江水陆交错带植物叶性状对水淹胁迫的响应及经济谱分析

以漓江水陆交错带为研究区,分两个条带分别量测了适生植物的5个叶性状指标:最大净光合速率(A_(max))、比叶重(LMA)、单位质量叶片全氮含量(N_(mass))、单位质量叶片全磷含量(P_(mass))、单位质量叶片全钾含量(K_(mass))。研究重度淹没带与微度淹没带不同功能型植物叶性状间的差异,分析并讨论重度淹没带叶性状间的关系与全球尺度是否存在差异,探究重度淹没带植物对水淹生境的生理响应机制。结果如下:(1)重度淹没带植物叶片的A_(mass)、N_(mass)、P_(mass)显著高于微度淹没带。(2)乔木、灌木叶片的LMA均显著高于草本植物,而A_(mass)、PPUE均显著低于草本植物。(3)重度淹没带草本叶性状指标的N_(mass)、P_(mass)、PNUE均显著高于微度微度淹没带,而乔木、灌木的叶性状在两个条带的差异则不显著。(4)重度淹没带植物叶性状关系与全球尺度基本一致,其植物叶片具有低LMA,高A_(mass)、Nmas s、P_(mass)。分析可知,重度淹没带植物在出露期提高叶片光合效率及相关营养水平可能是其适应水淹胁迫特殊生境的关键策略之一;不同功能型植物对同一环境的适应能力存在一定的差异,草本对于水淹环境的响应更为积极,适应能力更好;重度淹没带也存在叶经济谱,其植物在经济谱中属于"快速投资-收益"型物种。     

Acclimation of a terrestrial plant to submergence facilitates gas exchange under water

Flooding imposes stress upon terrestrial plants since it severely hampers gas exchange rates between the shoot and the environment. The resulting oxygen deficiency is considered to be the major problem for submerged plants. Oxygen microelectrode studies have, however, shown that aquatic plants maintain relatively high internal oxygen pressures under water, and even may release oxygen via the roots into the sediment, also in dark. Based on these results, we challenge the dogma that oxygen pressures in submerged terrestrial plants immediately drop to levels at which aerobic respiration is impaired. The present study demonstrates that the internal oxygen pressure in the petioles of Rumex palustris plants under water is indeed well above the critical oxygen pressure for aerobic respiration, provided that the air‐saturated water is not completely stagnant. The beneficial effect of shoot acclimation of this terrestrial plant species to submergence for gas exchange capacity is also shown. Shoot acclimation to submergence involved a reduction of the diffusion resistance to gases, which was not only functional by increasing diffusion of oxygen into the plant, but also by increasing influx of CO₂, which enhances underwater photosynthesis.