Response of cool-season grain legumes to waterlogging at
flowering
Silvia Pampana1, Alessandro Masoni, and Iduna Arduini
Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy
1To whom correspondence should be addressed (e-mail: silvia.pampana@unipi.it).
Short title: PAMPANA ET AL. - RESPONSE OF GRAIN LEGUMES TO WATERLOGGING 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
Soil flooding and submergence, collectively termed waterlogging, are major abiotic stresses, which severely constrain crop growth and productivity in many regions. Cool-season grain legumes can be exposed to submersion both at the vegetative and reproductive stages. Limited research has been carried out on these crops with waterlogging imposed at flowering. We evaluated how waterlogging periods of 0, 5, 10, 15, and 20 days at flowering affected seed yield, biomass of shoots, roots and nodules, and N uptake of field faba bean (Vicia faba L. var. minor), pea (Pisum sativum L.), and white lupin (Lupinus albus L.). Field Faba bean tolerated submersion better than pea and white lupin. Pea and white lupin plants did not survive 10 days of submersion, and after 5 days the seed yield, shoot and root biomass and N uptake had more than halved. Field Faba bean survived 20 days of waterlogging although seed and biomass production and total N uptake were severely reduced. Shoot dry weight and seed yield decreased linearly with the duration of waterlogging, which negatively affected seed more than the vegetative plant part weight. In all three crops waterlogging at flowering led to damage, which could not be recovered during seed filling.
Key words: waterlogging, legumes, flowering, duration, yield, roots, N content
La stagnation superficielle et souterraine représente l'un des principaux facteurs de stress abiotique qui limite fortement la croissance et la productivité des cultures dans 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47
beaucoup des régions. Les légumineuses à grains automnales peuvent être exposées à la stagnation dans la phase et végétative et reproductive. L’étendue de la recherche des effets de la stagnation imposée au moment de la floraison sur ces cultures a été vraiment limitée. Par conséquent nous avons évalué comment les périodes de stagnation imposées à 0, 5, 10, 15 et 20 jours de la floraison influencent la production des grains et de la biomasse de tiges, racines et des nodules ainsi que l’absorption de N par la féverole (Vicia faba L. var. minor), le pois (Pisum sativum L.) et le lupin blanc (Lupinus albus L.). La féverole peut tolérer la submersion bien plus que le pois et le lupin blanc. Les plants de pois et de lupin n’arrivent pas à survivre au delà de 10 jours de stagnation et, après 5 jours, la production des grains est réduite de moitié, ainsi que la biomasse de tiges et racines et l’absorption de N. La féverole peut survivre à 20 jours de submersion, même si la production des grains et des biomasses, comme l’absorption de N sont fortement réduits. Le poids sec des tiges et la production des grains décroissent linéairement avec la durée de la stagnation, ce qui influence négativement le poids des grains par rapport à la partie végétative. La stagnation cause aux trois cultures des dommages qui ne pourront pas être réparés avec le remplissage des grains.
Mots clés: stagnation, légumineuses, floraison, durée, production, racines, teneur en N 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71
Soil flooding and submergence, collectively termed waterlogging, are major abiotic stresses, which severely constrain crop growth and productivity in many regions. Waterlogging causes soil oxygen deficiency, which inhibits root respiration leading to decreased shoot and root growth (Jackson and Drew 1984; Jayasundara et al. 1998; Rhine et al. 2010). In legumes, waterlogging can reduce photosynthesis, plant growth, grain yield, the formation, function and survival of nodules, biological nitrogen fixation (BNF), and cause plant death during or some weeks after the end of waterlogging (Minchin and Summerfield 1976; Bacanamwo and Purcell 1999; Davies et al. 2000).
The impact on legumes of a waterlogging event depends on the stage of growth and duration of submergence (Jayasundara et al. 1998). The ability to survive and recover following waterlogging generally decreases with increasing plant age and declines sharply as reproductive growth approaches (Jayasundara et al. 1998). Waterlogging duration has been recognised as a major factor in plant survival following oxygen deprivation stress (Striker 2008), and the reduction in plant growth increases with the length of the waterlogging period.
Management practices to reduce the effects of waterlogging include the species choice and the proper design of field drainage systems to discharge excess water. The knowledge of the waterlogging tolerance of legumes assists agronomists to choose the best legume to grow and to determine the required characteristics of the drainage system (e.g. volume, depth and spacing of drains). Waterlogging affects all grain legumes, however the capacity to tolerate it varies: faba bean is the most tolerant, followed by the 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95
relatively tolerant cowpea, soybean, field bean and pea and finally chickpea (Minchin and Summerfield 1976; Jackson 1979; Siddique et al. 2000; Solaiman et al. 2007). Waterlogging is especially dangerous for cool-season grain legumes, which can be exposed to submersion both at the vegetative stage and at the beginning of reproduction. Limited data are available on the seed yield loss resulting from waterlogging in cool-season grain legumes and very little research has been carried out with waterlogging imposed at flowering. However in field faba bean, pea and chickpea, the reductions in grain yield can vary from negligible to almost 100% depending on the growth stage when plants are waterlogged and the duration of the stress (Jayasundara et al. 1998).
Our aim was to evaluate how waterlogging imposed at the beginning of flowering affects the shoot and root growth and seed yield of field faba bean, pea, and white lupin.
MATERIALS AND METHODS
Site Characteristics and Experimental Design
The research was carried out from November to July in two consecutive years (2013 and 2014), at the Research Centre of the Department of Agriculture, Food and Environment of the University of Pisa, Italy, which is located at a distance of approximately 10 km from the sea (43° 40′ N, 10° 19′ E) and 1 m above sea level. According to Köppen The the climate of the area is hot-summer Mediterranean (Csa) with mean annual maximum and minimum daily air temperatures of 20.2°C and 9.5°C respectively, and a mean cumulative rainfall of 971 mm per year.
In each year, experimental treatments consisted of three legume crops and five periods of waterlogging treatments imposed at the beginning of flowering. The legume crops were field faba bean (Vicia faba L. var. minor) cv. Chiaro di Torrelama, pea 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118
(Pisum sativum L.) cv. Iceberg, and white lupin (Lupinus albus L.) cv. Multitalia. The five waterlogging treatments were one durations of waterlogging were 0 (well-drained control and four waterlogging durations of), 5, 10, 15, and 20 days. Five to 20 days of waterlogging were used because preliminary experiments on field faba bean showed that they induced severe waterlogging symptoms but did not actually kill the plants.
Experimental Equipment and Crop Management
Plants were grown in boxes of 0.50 x 0.50 m and 0.6 m depth, spaced 20 cm apart, and embedded in expanded clay to avoid daily fluctuations in soil temperature. A 50 mm diameter hole was drilled in the bottom of each box. In each year a total of 75 boxes were used (5 waterlogging periods x 3 species x 5 replicates). In both years, approximately six months before seeding, growth boxes were filled with soil collected from a field previously cultivated with rapeseed. The main properties of the soil were similar in the two years and were approximately: 74.8% sand (2 mm > ∅ > 0.05 mm), 21.9% silt (0.05 m > ∅ > 0.002 mm), 3.3% clay (∅ < 0.002 mm), 8.1 pH (saturated paste method), 1.5% organic matter (Walkley and Black method), 0.6 g kg-1 total nitrogen (Kjeldahl method), 11.9 mg kg-1 available P (Olsen method), and 122.1 mg kg-1 available K (BaCl2-TEA method).
Crops were sown on 20 November 2012 and 18 November 2013, within the optimum planting time for cool-season legume production in central Italy. Before sowing, field faba bean and pea seeds were inoculated with Rhizobium leguminosarum biovar. viciae, and white lupin seeds with Bradyrhizobium lupinus. The seeding rate was 56 seeds m-2 (14 plants per box) for field faba bean and pea, and 40 seeds m-2 for white 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142
lupin (10 plants per box). For all crops, a 30-cm row spacing was used. Before planting, all legume crops were fertilised with urea, triple mineral phosphate and potassium sulphate, at rates of 30 kg ha-1 of N, 65 kg ha-1 of P and 125 kg ha-1 of K. The crops were kept free of weeds by hand hoeing when necessary.
The beginning of flowering occurred on 29 March 2013 and 13 March 2014 for field faba bean and on 3 April 2013 and 20 March 2014 for pea and white lupin. Waterlogging was imposed by placing boxes into containers (10 m x 2.5 m x 0.8 m) with a 3 cm layer of free water above the surface of the box throughout the period of each waterlogging treatment (in this condition the soil in the boxes was completely saturated by water). At the end of each waterlogging period, boxes were taken out of the containers and remained without irrigation for 10 days, and left to drain freely, after which they were maintained near to field capacity until the plants reached maturity. Control boxes were watered near to field capacity throughout the growing season.Waterlogging treatments consisted of raising the water level of the growth boxes to approximately 3 cm above the soil surface. Before and after being waterlogged, all the boxes were maintained in well-watered drained conditions until plant maturity.
Sampling Procedures and Measurements
Crops were harvested at maturity: 4 July 2013 and 23 June 2014 for pea and field faba bean, and 8 July 2013 and 1 July 2014 for white lupin. Waterlogging did not influence the cycle length of the three legume crops and the maturity stage was simultaneously reached in both surviving waterlogged and control plants. All Plants plants from each box were manually cut at ground level and aerial parts were partitioned into shoots and pods. The number of pods was counted, pods were divided into pod walls and seeds, 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166
and seed yield and mean seed weight were recorded. Roots were separated from the soil by gently washing by a low flow from sprinklers in order to minimise loss or damage. Nodules were subsequently separated from the roots; fresh weight and number were recorded. One sample of roots was stored in a refrigerator until the length of the roots was estimated with the line intersection method (Tennant 1975). For dry weight determination, samples of all plant parts were oven dried at 60°C to constant weight. All plant parts were analysed for nitrogen concentration (Kjeldahl method), and N contents were calculated.
Statistical Analysis
Results were subjected to analysis of variance. The effect of year, waterlogging duration, crop, and their interactions were analysed using a split-split-plot design with year designed as whole plots, waterlogging duration as sub-plots and crop as sub-sub-plots. Significantly different means were separated at the 0.05 probability level by the least significant difference test (Steel et al. 1997).
RESULTS AND DISCUSSION
Weather ConditionsDaily minimum and maximum temperatures and rainfall during both growing seasons were obtained from a meteorological station located within 100 m from the trial site. The weather during the experiment was typical of the autumn-spring growing season in central Italy and maximum and minimum temperatures did not differ from the 20-year average for the area and were similar in the two years (Fig. 1). During the legume growing season the daily mean temperature was 11.6°C in 2013 and 12.7°C in 2014. 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190
The heat accumulated over both the vegetative (1,014°C in 2013 and 1,055°C in 2014) and the reproductive periods (1,736°C in 2013 and 1,760°C in 2014) were very similar in the two years. Rainfall was 1,130 mm in 2013 and 855 mm in 2014. Compared with 2014, 2013 had more precipitation before the flowering stage, while after flowering the two years had similar values (153 and 194 mm).
Despite the different rainfall conditions between the two years, the analysis of variance revealed no significant differences between years or “Year x Waterlogging duration x Crop” interaction, “Year x Waterlogging duration” interaction, “Year x Crop” interaction for all the parameters measured. Accordingly, the following results are averaged over the two years.
Seed and Shoot Dry Weight
Field Faba bean overall exhibited a higher tolerance to waterlogging than pea and white lupin. Although all three crops showed the same symptoms of excessive water stress, in pea and white lupin, the plant response was more rapid than in field faba bean, and after only 24 hours they showed a general yellowing of the leaves, shoot wilting, and abscission of leaflets of lower leaves. In the subsequent 4-5 d of waterlogging, pea and white lupin showed abscission of leaflets of the other leaves, cessation of flowering, and death of many recently opened flowers. Similar symptoms have been recorded in chickpea, grasspea, lentil, mungbean, pea, pigeon pea, and soybean (Takele and McDavid 1995; Cowie et al. 1996b; Bacanamwo and Purcell 1999; Kumar et al 2013; Malik et al. 2015) other legumes. Shoot wilting seems to be a common feature of plants subjected to waterlogging (Cowie et al. 1996a), which has been attributed to higher resistance to mass flow of water through the roots (Jackson and Drew 1984). Yellowing 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214
of the plant might be due to a reduction in leaf nitrogen, caused by the cessation of biological nitrogen fixation during waterlogging, or to the production of toxic substances, such as nitrites and sulphides, which move from the soil through roots to the leaves (Kumar et al. 2013) or .of reactive oxygen species (ROS), which cause severe damage to membranes, DNA and proteins in plant cells (Ahmed et al. 2002).
Five days of waterlogging led to the death of 30% of white lupin plants and 10 d led to the death of all pea and white lupin plants. In both treatments plant death occurred during the 7 d following the end of waterlogging. These results are in accordance with Cowie et al. (1996a) who observed that chickpea plants were unable to recover when waterlogging was imposed 6 d after flowering had begun. In field faba bean, the symptoms of waterlogging stress appeared with about 10 d of waterlogging and all plants survived even with 20 d of submersion.
After five days of waterlogging, white lupin plants were infected by Macrophomina phaseolina, which is one of the most damaging seed and soil borne pathogens (Srivastava and Singh 1990). Field Faba bean and pea plants remained disease-free throughout the entire experiment.
Shoot dry weight (stems + leaves + pod walls) of pea and white lupin plants waterlogged for five days was 52-60% lower than the control (Fig. 2). In field faba bean shoot dry weight decreased progressively with the increase in waterlogging duration, and with 20 days of submersion there was a 41% reduction. Despite with 5 d of waterlogging field faba bean plants did not show visible symptoms of stress, at maturity shoot dry weight was significantly lower than control.
Five-day waterlogging reduced seed yield of pea and white lupin by 60% in comparison with control (Fig. 2). In pea, the lower grain yield was due to a reduction in 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238
both the number of seeds per plant and mean seed weight, while in white lupin, this was only due to the number of seeds per plant (Table 1). In field faba bean, seed yield progressively decreased with an increased duration of waterlogging and was halved by the 20-day long waterlogging (Fig. 2). Similarly to pea, in field faba bean the reduction in seed weight was due to both the number of seeds per plant and mean seed weight. Our results on field faba bean are in accordance with Scott et al. (1989) who found that shoot dry weight and seed yield of soybean decreased linearly with the duration of waterlogging at flowering.
In all crops, the decrease in the number of seeds per plant was related to the number of pods per plant, while the number of seeds per pod was unchanged by waterlogging. Therefore, in all legumes, waterlogging markedly affected the number of flowers per plant but did not affect the number of eggs per flower. The reduction in mean seed weight observed in pea and field faba bean was probably due to a decrease in photosynthesis and nitrogen supply to seeds (BNF and N remobilisation) during seed filling, both resulting from reduced shoot and nodulated root growth. This finding is confirmed by the shoot/seed ratio, which increased in all three crops with the increase in waterlogging duration. This thus showed that waterlogging negatively affected seed more than the vegetative plant part weight.
Root and Nodule Dry Weight
In barley, faba bean, lupin, pea, and soybean The the submersion of soil reduces the growth of roots by inhibiting aerobic respiration (Jackson and Drew 1984, Bacanamwo and Purcell 1999; Davies et al. 2000). In our researchpea and white lupin, waterlogging affected both taproot and rootlets of pea and white lupin. At maturity, the taproot of 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262
both crops when waterlogged had a lower dry weight than the control by about 35%, and rootlets by about 25%. Waterlogging also reduced the length of the roots of these crops, which with 5 d of submersion was approximately one-third lower than control. The taproot of field faba bean was more resistant to waterlogging than pea and white lupin since it was unaffected by 5-d submersion, however after 20 d of waterlogging it was half the amount of the control. Waterlogging progressively reduced rootlet dry weight and length of field faba bean, which after 20 days were about one-third of the control (Fig. 3). These findings confirm that waterlogging causes the dieback of the primary root system of legume species (Henshaw et al. 2007) and show that the period subsequent to submersion is not sufficient for a full recovery of the roots. Lentil, field pea, soybean and faba bean produce aerenchyma within roots to facilitate the aeration of flooded tissue (Thomas et al. 2005; Stoddard et al. 2006; Solaiman et al. 2007). Waterlogged plants of faba bean, soybean, and mungbean produce adventitious roots to enhance oxygen transport from the stem to the roots and to reduce flooding injury (Henshaw et al. 2007; Solaiman et al. 2007; Islam et al. 2010). We monitored the root system only at maturity and did not observe adventitious roots in any of the crop. Probably this is because the development of adventitious roots is related to better O2 supply near the soil surface (Jackson and Drew 1984) while in our research water was maintained 3 cm above the soil surface.
The species utilized in this research, faba bean, pea and white lupin, have indeterminate nodules with irregular size, shape, and clustering, which is a consequence of indeterminate growth allowed by a persistent meristem (Sprent 1980). Relatively little information is available on nodulation in cool season grain legumes in responses to waterlogging. However the reduced root growth, particularly loss of root hairs under 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286
waterlogging, may inevitably reduce nodule initiation. In pea and white lupin, 5-day waterlogging approximately halved the number of nodules and reduced their weight by one-third (Fig. 4). In field faba bean, the nodule number and weight decreased with the increase in waterlogging duration. Both parameters were affected by waterlogging already after 5 d (about 80% of control) and were approximately half the amount of the control after 20 d. The nodule cutback during waterlogging could be partially attributed to the dieback of the root system and partially to the detachment of nodules resulting from the reduction in energy supply from shoots to nodules. In all crops, mean nodule weight increased with increasing periods of waterlogging, thus showing that the small nodules had been detached during submersion (Fig. 4). In all crops, however, we found that the ratio between nodule dry weight and number (mean nodule weight) increased with waterlogging duration, which is consistent with the hypothesis that the smaller nodules were preferentially detached during submersion (Fig. 4).
Nitrogen Concentration and Content
In all crops waterlogging did not affect nitrogen concentration in any of the plant parts. Accordingly, the reductions in N content of different plant parts were similar to those of the dry weight (data not shown). Five-day long soil waterlogging reduced total N uptake by 57% in pea and 69% in white lupin (Fig. 5). In field faba bean, total N uptake reduction after five days of waterlogging was only 17%, however it increased to 48% with prolonged waterlogging up to 20 days.
Jayasundara et al. (1998) reported that waterlogging markedly reduces the N uptake in field bean, lentil, chickpea and faba bean and this reduction appears at least partly responsible for the premature chlorosis and leaf senescence of waterlogged plants. In 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310
cool-season grain legumes BNF represents more than 80% of N uptake from flowering to maturity (Pampana et al. 2015). In cowpea and soybean, waterlogging decreased BNF relatively more than biomass accumulation, and the decrease in BNF was responsible for decreased vegetative growth and nitrogen content (Minchin and Summerfield 1976; Bacanamwo and Purcell 1999). Biological nitrogen fixation measurements were not taken in this study, however the large reduction in both nodule number and dry matter indicated that waterlogging was likely to have reduced BNF. Moreover, Pampana et al. (2015) showed that remobilised N supplies half of seed N content at maturity in pea and white lupin and one third in fabafield bean. The abscission of leaves and the dieback of roots caused by waterlogging may have reduced the amount of remobilised N.
In conclusion, waterlogging imposed at flowering markedly affected seed yield and biomass of shoots, roots and nodules of all three legume crops but field faba bean tolerated submersion stress better than pea and white lupin. The growth of the latter two crops had markedly decreased already with only five days of submersion, and died with more than five days. Field Faba bean survived even with 20 d of waterlogging although its seed and biomass production were severely reduced. Faba bean continued to retain nodules, but these tended to be only the larger nodules. These findings highlight that in all three crops, waterlogging at flowering damaged the plant growth, which could not be recovered during seed filling.
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Figure captions
Fig. 1. Rainfall, maximum, and minimum temperature in 2012-2013 and 2013-2014. Fig. 2. Seed and shoot dry weight. Crop x waterlogging duration interaction. In this and following figures vertical bars represent LSD (P≤0.05).
Fig. 3. Taproot and rootlet dry weight and root length. Crop x waterlogging duration interaction.
Fig. 4. Nodule dry weight and number and mean nodule weight. Crop x waterlogging duration interaction.
Fig. 5. Total nitrogen content. Crop x waterlogging duration interaction. 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430
Table 1. Seed yield components. Crop x waterlogging duration interaction.
Crop Waterlogging
duration
Pod number Seed per pod Seed number Mean seed weight (d) (n plant-1) (n pod-1) (n plant-1) (mg) Field Faba bean 0 16.4b 3.0a 49.3b 448.8a 5 15.6bc 3.0a 46.9bc 391.9b 10 13.9c 2.5a 35.0cd 384.2b 15 10.4d 3.0a 30.7d 380.8b 20 10.9d 2.7a 29.4de 346.4c
Pea 0 20.1a 4.4a 87.8a 186.2f
5 11.0d 4.2 a 46.4bc 110.1g
White lupin 0 11.6d 4.0a 46.7bc 278.5d
5 4.2e 3.8a 15.9e 253.7e
Values followed by different letters within columns are significantly different (P<0.05) 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445
Fig. 2. Seed and shoot dry weight. Crop x waterlogging duration interaction. Vertical 447 448 449 450 451 452 453 454
bars represent LSD (P<0.05).
Fig. 3. Taproot and rootlet dry weight and root length. Crop x waterlogging duration 455 456 457 458 459 460 461 462
interaction. Vertical bars represent LSD (P<0.05). 463
Fig. 4. Nodule dry weight and number and mean nodule weight. Crop x waterlogging duration interaction. Vertical bars represent LSD (P<0.05).
465 466
Fig. 5. Total nitrogen content. Crop x waterlogging duration interaction. Vertical bars represent LSD (P<0.05). 0 5 10 15 20 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 Faba bean Pea White lupin
