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Article

Evaluation and Selection of Bromegrass Genotypes under Phosphorus and Water Scarcity towards the Development of Resilient Agriculture Focusing on Efficient Resource Use

by
Sebastián Meier
1,2,*,
Pedro M. de Souza Campos
1,
Arturo Morales
1,
Rafael López-Olivari
1,
Fernando Ortega-Klose
1,
Humberto Aponte
3,
Paula Cartes
4,
Naser Khan
5,
Gabrijel Ondrasek
6,
Pamela Cea
7,
Rubén Palma-Millanao
8 and
Alex Seguel
9,*
1
Instituto de Investigaciones Agropecuarias, INIA Carillanca, Casilla Postal 929, Temuco 4880815, Chile
2
Escuela de Agronomía, Facultad de Ciencias, Ingeniería y Tecnología, Universidad Mayor, Campus Alemania Sede Temuco, Temuco 4801043, Chile
3
Laboratory of Soil Microbial Ecology and Biogeochemistry, Institute of Agri-Food, Animal and Environmental Sciences (ICA3), Universidad de O’Higgins, San Fernando 3070000, Chile
4
Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, Temuco 4811230, Chile
5
School of Chemical Engineering, University of Adelaide, Adelaide, SA 5000, Australia
6
Faculty of Agriculture, The University of Zagreb, Svetosimunska c. 25, 10000 Zagreb, Croatia
7
Carrera de Biotecnología, Facultad de Ciencias Agropecuarias y Medioambiente, Universidad de La Frontera, Temuco 4811230, Chile
8
Vicerrectoría de Investigación y Postgrado, Universidad de La Frontera, Temuco 4811230, Chile
9
Departamento de Ciencias Agronómicas y Recursos Naturales, Facultad de Ciencias Agropecuarias y Medioambiente, Universidad de La Frontera, Temuco 4811230, Chile
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(1), 121; https://doi.org/10.3390/agronomy14010121
Submission received: 11 November 2023 / Revised: 25 November 2023 / Accepted: 27 November 2023 / Published: 3 January 2024
(This article belongs to the Section Water Use and Irrigation)
Browse Figures
Versions Notes

Abstract

:
The relationship between phosphorus (P) availability and water restriction was explored in this study, focusing on its impact on phosphorus use efficiency (PUE) and water use efficiency (WUE) in various bromegrass (Bromus spp.) genotypes. Under controlled conditions, five bromegrass genotypes, as well as one ryegrass (Lolium perenne) cultivar, were compared by subjecting them to two P levels and two watering regimes. It was determined that combining water and phosphorus limitations led to reduced plant productivity. Initially, the ryegrass outperformed the bromegrass, but this result declined over time, while bromegrass exhibited consistent stability. Notably, under P and water stress, enhanced root development was observed in bromegrass compared to that in ryegrass. Distinct patterns of PUE and WUE allowed for the categorization of bromegrass genotypes into three groups. Genotype 3457 emerged as the most efficient, scoring 20 out of 24, while Pro 94-49 A achieved a score of only 10 out of 24. This study suggests that the drought resilience of bromegrass may be linked to increased root growth during the early vegetative stages, which potentially facilitates improved P acquisition. However, further validation through long-term field experiments is needed. The insights from this study are potentially valuable for use in shaping plant breeding programs by revealing the plant adaptation mechanisms for both P and water absorption.

1. Introduction

Drought is a significant limitation to the productivity of agricultural systems and food production worldwide [1,2]. The reduction of precipitation and the modification of rainfall patterns due to climate change are causing widespread water deficits worldwide, producing negative impacts on plant growth, which in turn, cause a substantial decline in crop yield [2]. In this sense, water deficit stress triggers a series of physiological plant responses, including reduced growth and respiration rates and stomatal closure, thereby reducing the rate of water loss from transpiration [3,4,5]. Stomatal closure simultaneously reduces the rate of photosynthesis, limiting carbon fixation and the availability of carbohydrates for plant maintenance [6,7,8]. Ultimately, prolonged water deficit stress has significant adverse effects on growth and physiological processes, potentially leading to decreased fitness, complete reproductive failure, or mortality, making water deficit stress a critical selective agent in both natural and cultivated plant populations [5,9,10]. One trait that is important in plant response to water deficit stress is water use efficiency (WUE).
The definition of WUE depends on the measurement scale and the units of exchange being considered [11]. All potential definitions involve some measure of water being exchanged for some unit of target production. At the plant level, WUE corresponds to the ratio of plant dry weight (DW) and water use (WU) through plant transpiration [7]. If under future climate scenarios, agricultural production will be constrained by WU reductions in rainfed systems, then the selection of genotypes with a higher WUE should be the target in order to attenuate the negative impact of water deficit stress on plant yield [12].
On the other hand, phosphorus (P) is critical to crop productivity. Despite P being relatively abundant in many soils, it is largely unavailable for plant uptake because P forms insoluble complexes with cations under acid and alkaline conditions [13,14,15]. As a result, large amounts of phosphate fertilizers been applied since the Green Revolution to sustain the production of agricultural systems [16,17]
Phosphorus use efficiency (PUE) is “the dimensionless ratio of the mass of harvested P in agricultural products to the mass of total P inputs in this” [18]. The PUE is the product of P uptake efficiency (PUPE) and P utilization efficiency (PUTE) [19,20]. PUPE refers to the ability of crops to absorb P from soils at a given P supply, whereas PUTE involves the optimization of its internal utilization [21]. Therefore, in the crop production systems, PUE is an essential indicator for measuring the status of P management in the agricultural production system, as well as its impacts on food security and environmental conservation [18,22].
The current scientific evidence shows that P application appears to mitigate the burden caused by water deficit stress [23,24]. Indeed, the adaptive plant strategies to acquire and utilize P are related to those to access more water, suggesting the existence of an interaction between both strategies. Recently, Refs. [25,26] identified an interactive role between phosphorus use efficiency (PUE) and WUE in winter and spring wheat genotypes, opening up the possibility of selecting P-efficient wheat genotypes that will also exhibit efficient water use, constituting a new approach to overcome water deficit stress and promote food security under future climate change scenarios.
Bromegrasses (Bromus spp.) comprise a broad group of annual, biennial, and perennial grasses [27], some of which have been partially domesticated [28]. Some species are native to Chile, with a wide distribution in the Chilean and Argentinean Andes [29]. The genus includes valuable forages and weedy species [30]. According to Matthei [31], 24 species are present in Chile, and only 4 are considered forages of economic importance. Bromegrass exhibits agronomic characteristics similar to those of perennial ryegrass (Lolium perenne L.), but with higher biomass production and herbage quality. However, bromegrass produces more dry matter during periods of soil water limitation, such as those occurring during summer [32]. The above may indicate functional compatibility between perennial ryegrass and bromegrass, which benefits the pasture because the brome can continue to grow under water deficit conditions [33]. This is critical in the selection and genetic breeding of bromegrass, leading to the establishment of cultivars from wild accessions [34].
Some studies have evaluated the effect of P fertilization on brome growth and development [35,36,37,38]. There is also evidence regarding the tolerance of this species to water deficit stress [30,39,40]. However, to our knowledge, no studies have evaluated the reaction of this bromegrass to the combination of phosphorus and water deficit stress in order to categorize and select efficient genotypes relating to both resources. This research aimed to evaluate the effects of P and water scarcity OVER PUE and WUE for categorizing co-adapted brome genotypes for future plant breeding.

2. Materials and Methods

Five brome genotypes, including one cultivar: Bronco (Bromus valdivianus), two advanced lines: 3287 (B. valdivianus) and 3771 (B. coloratus), and two accessions: PRO 94-49 A (B. lithobius) and 3457 (B. coloratus), were used to evaluate their response to P and water deficit stress (Table 1). In addition, Lolium perenne (Nui cv.) was utilized as a reference to compare the performance of Bromus, a drought-tolerance plant [30,40], with that of a species presumably not adapted to water deficit stress [40]. Nevertheless, PUE and WUE were categorized only according to the information provided for the Bromus genotypes.
An agricultural volcanic soil, Barros Arana series, which is medial, mesic, Typic Hapludand soil [41], was collected from the La Araucanía Region (Southern Chile, 39°06′ S 72°41′ W) and characterized physiochemically (Table 2). The experiment was conducted at the Instituto de Investigaciones Agropecuarias Regional Research Center Carillanca (INIA-Carillanca), Región de La Araucanía, Chile (38°41′ S, 72°25′ W).

2.1. Plant Growth Conditions and Analysis

The soil was air-dried, ground, and sieved up to 5 mm. Two P treatments were assessed: low P concentration—4 mg P kg−1 (−P); and high P concentration—30 mg P kg−1 (+P). The samples were enriched using triple super-phosphate (46% P2O5), according to the methods of Etchevers et al. [42].
The bromegrass seeds were disinfected by immersion in 2.5% (v/v) of Tebuconazole and Prothioconazole (Raxil 0.60, Bayer, Germany), sowed in a seed starter tray (128 holes 40 cm × 29 cm × 56 cm), and allowed to grow until they reached a height of 7 cm. Then, six plantlets were transplanted to 7 L soil polythene-lined plastic pots (20 cm × 20 cm × 25 cm), filled with 4 kg of the previously described soil.
Nitrogen was supplied using urea in an equivalent dose of 180 kg N ha−1, split into six applications as follows: at plant establishment, an equivalent of 60 kg N ha−1 was applied, and after every defoliation, an equivalent of 20 kg N ha−1 was applied. Potassium was added at plant establishment, providing an equivalent dose of 120 kg K2O ha−1 using KSO4.
Two irrigation treatments were imposed: well-watered (+W) and water-stressed (−W). The water-stressed plants received 30% of the water applied to +W samples. The amount of water applied to the +W samples was determined based on the total available soil water (TAW; mm), the soil water depletion fraction (p), and the readily available soil water (RAW; mm). In this study, a value of p = 0.6 was used, in accordance with the values proposed by Allen et al. [43] for Gramineae. Irrigation was applied to the +W samples when 60% of the TAW was removed (Figure 1). Irrigation frequency was determined using frequency-domain reflectometry (FDR) sensor data (the 5 MT from Decagon Devices, Inc., Pullman, WA, USA).
The signal was recorded at 15 min intervals using a datalogger (ZL6, METER Group, Inc., Pullman, WA, USA). The irrigation time was determined by RAW, the flow rate of the emitters, and the irrigation efficiency. For treatments −W and +W, pressure compensating button drippers (Netafim Ltd., Tel Aviv, Israel) were used in each pot, with a 1.2 and 4.0 L/h flow discharge, respectively. The plants were grown in a greenhouse (14/10 h light/dark photoperiod) with open windows to simulate field conditions but prohibit rainwater entrance.
The pasture defoliation frequency was based on the leaf regrowth stage (LS) and was performed when the +P-treated plants exhibited four fully expanded leaves (LS-4, expansion of four sequential leaves per tiller), according to the methods of Ordóñez et al. [32]. When a treatment reached the LS4 stage, the tillers were cut to a height of 3 cm above ground level. The defoliation of the L. perenne plants was performed simultaneously with that applied to the Bromus samples. Six defoliations were performed (Figure 1 and Figure S1, Supplementary Materials). The entire plant (shoots and roots) was separated and harvested at the final cut. The shoots and roots were washed with Milli-Q water after separation, and then dried in a forced-air oven at 70 °C for 48 h, followed by weighing. The samples were ground, incinerated at 550 °C, and digested using an H2O-HCl-HNO3 mixture (8/1/1, v/v/v). Using the vanadate-molybdate method, the P concentration was measured using spectrophotometry [44]. The phosphorus uptake was calculated as the product of the P concentration and the dry weight of the shoots and/or roots.
Phosphorus use efficiency (PUE) was calculated according to the methods of Moll et al. [19] as the product of phosphorus uptake efficiency (PUPE) and phosphorus utilization efficiency (PUTE). The equations used were as follows:
PUE (g DW g−1 P supply) = DW/P supply
PUPE (g P uptake g−1 P supply) = P uptake/P supply
PUTE (g DW g−1 P uptake) = DW/total P uptake
The P supply was estimated as the sum of the potential soil P supply at sowing (in the −P treatments) plus P fertilization (in the +P treatments) [45].
The water use efficiency of the plant (WUE) was calculated according to the methods of Meena et al. [12]
WUE (g pot L−1) = DW/water applied
The categorization of brome genotypes for PUE and WUE was performed according to the methods proposed by Aziz et al. and Bilal et al. [46,47]. The Bromus genotypes were classified into three categories: (i) efficient (E), (ii) medium (M), and (iii) inefficient (I). The genotypes were labeled as efficient if their PUE or WUE mean was higher than the mean plus standard deviation of the total population of genotypes evaluated (>μ + SD), medium if their mean was between μ − SD and μ + SD, and inefficient if their PUE or WUE mean was inferior to the mean less the standard deviation of the entire Bromus population (<μ − SD).

2.2. Data Analysis

The experimental design consisted of a completely randomized split-split-plot arrangement, in which the main plot was assigned to the water irrigation treatment (well-watered and water-stressed: +W and −W, respectively), and the soil P concentrations were designated as the sub-plot factor (−P: 4 mg P kg−1 and +P: 30 mg P kg−1); the Bromus and the L. perenne genotypes were identified as the inner factor. The experiment was conducted with three replicates per treatment (n = 72). A multifactorial analysis of variance (ANOVA) was performed to estimate the F-value of each factor and its interactions. The means of the genotypes were compared for each of the four combination treatments (W × P) through a one-way analysis of variance (ANOVA) and Tukey’s honestly significant difference (HSD) test. The normality of the residuals and variance homoscedasticity were tested using Shapiro–Wilk’s and Levene’s tests, respectively. Data analyses were performed using Infostat software v.2020e [48].

3. Results

Most of the analyzed variables were dependent (p ≤ 0.05) on the phosphorus treatment (P), the Bromus genotype (G), and the irrigation level (W) (Supplementary Table S1). The P treatment was responsible for the totality of the parameters analyzed, whereas G and W explained most of the responses (9 out of 11 variables each). High interactions between GxP and WxP were observed (9 out of 11 variables each). However, there were few interactions between GxW (5 out of 11). Finally, the triple interaction of GxWxP explained only 3 out of 11 analyzed variables.
The cumulative shoot growth of the Bromus genotypes varied in response to both P and water application, except in the +W+P condition (Figure 2). The lowest plant performance was observed when both P and water restrictions were jointly applied (−W−P, Figure 2A). The additional water increased the shoot growth 2.3 and 2.1 times in the −P and +P samples, respectively (mean of all Bromus genotypes, Figure 2). Slightly less marked effects were observed due to the addition of P (+P), which produced an increase in shoot growth of 2.0 and 1.8 times in −W and +W, respectively (the mean of all Bromus genotypes, Figure 2). Nevertheless, minor differences among Bromus genotypes were observed. For example, the genotypes 3457, 3287, and Bronco, under −P conditions, showed a shoot dry matter production similar to that obtained by Nui (L. perenne), independent of the amount of water applied (Figure 2A,B). In most cases, the genotype Pro94-49A exhibited the lowest performance in regards to shoot growth in nearly all treatments, except for in +W+P; under such conditions, no differences were observed among the genotypes (Figure 2D).
Different patterns regarding shoot biomass production were observed among plants during the growth period (Figure S1). Among the four treatments, Nui, the ryegrass used as a reference, produced more dry shoot matter than any Bromus genotype, especially during the three initial cuts. However, its performance declined after the fourth and fifth cuts; meanwhile, bromegrasses maintained their shoot growth rates (Figure S1). At the sixth cut, the shoot biomass production of Bromus was equivalent to or superior to that observed in Nui.
The addition of phosphorus and water also promoted root growth (Figure 2). On average, the root biomass production under non-restrictive conditions (+W+P) was almost 2.6 times higher than that observed under −W−P conditions. Nevertheless, no differences among genotypes were observed among the different treatments, with the exception of the +W+P treatment (Figure 2D). Under the above condition, the genotype Pro 94-49A showed the smallest root growth. In contrast, Nui showed a performance similar to that of the best Bromus performers under all treatments, except the −W−P condition, which displays the lowest performance regarding root growth (Figure 2A). On the contrary, under the +W+P condition, the root biomass production of Nui was notoriously higher than that of any of the bromegrass genotypes evaluated (Figure 2D).
Differing effects on shoot P concentration were observed among the genotypes and the treatments applied (Table S2). Broadly, the addition of P to the water-stressed treatments increased the P-concentration of the shoots by about 55% (compared with that of the −W−P treatment using the mean of all cuts of the five Bromus genotypes). The most responsive genotype to P addition in water-stressed conditions was Pro 94-49A, which increased their shoot P concentration by about 73% higher than −W−P. A similar effect was observed due to P addition to well-watered plants increasing shoot P concentration by about 37% (compared to +W−P). However, the additional water applied to plants growing with adequate P levels reduced the shoot P concentration by about 15% in the genotypes Pro 94-49A, 3457, and 3772 (compared to that of the +W−P samples, Table S2).
Similar results were observed in the root P concentration (Table S2). The addition of P to the plants under water deficit stress increased the root P concentration from 4% in the 3771 to 68% in the Pro94-49 genotype. The above effect was actually enhanced when water and P were jointly applied, increasing the root P concentration by about 78% (compared to the mean of all genotypes). However, a single water application to plants growing under P scarcity conditions decreased the P concentration in all Bromus genotypes except for Bronco. On the contrary, the water application to plants with high P concentrations increased the root P concentrations in the 3287, 3771, and Bronco genotypes.
The addition of P and water also increased the shoot P uptake in all the genotypes (Figure S2). Increasing the P concentration in the soil boosted the uptake of this element in a range of 2.5 and 3.3 times higher in the 3287 and Bronco genotypes, compared to that noted in the −W−P samples). The above trend was maintained as moderately constant when P and water were jointly applied. In addition, the single water addition (+W) to the P deficient treatments (−P) increased the plant P uptake by about 2.2 times (using the mean of five genotypes), excluding Bronco, which showed an increase of only 84% (compared to the −W−P samples). Finally, adequate water and P concentrations enhanced the shoot P uptake from 89% in the Bronco genotype to 2.3 times higher in genotype 3287 (Figure S2, Supplementary Materials).
The addition of P decreased the P uptake efficiency (PUPE) in all genotypes evaluated by about 56% and 63% in the −W and +W samples, respectively (using the mean of all Bromus genotypes, Table 3). On the contrary, the single water addition (+W) increased the PUPE by about 2.2 and 2.0 times in the water-stressed treatments in the −P and + P samples, respectively. The best performance in the −P condition was observed for genotype 3457, independent of the water applied, and in general, the lowest PUPE was observed for the genotype Pro 94-49A, except for in the +W+P samples, in which no differences in PUPE were observed among the Bromus genotypes (Table 3). Similarly, the addition of P to the water-stressed plant decreased the PUTE by about 37% and 32% in −W and +W, respectively (using the mean of all genotypes), with a similar performance among the Bromus genotypes, except for Pro 94-49A, which has the lowest PUTE of the group in the −W condition (Table 3).
Finally, the phosphorus and water use efficiency (PUE and WUE, respectively) varied in response to P and water under all conditions evaluated (Figure 3). For example, it can be observed that line 3457 used P and water efficiently under P scarcity, whereas the cultivar Bronco showed the best performance for PUE and WUE under +P conditions. Assessing all the conditions, the categorization of genotypes according to their PUE and WUE showed that line 3457 was the most efficient, with a total score of 20 out of 24 (Figure 4 and Figure 5, Table S3). Second place was achieved by the advanced lines 3287 and 3771, and the four treatments evaluated for all the Bronco genotypes ranked as “medium”. On the contrary, the Pro 94-49A genotype was inefficient under nearly all conditions, except for the +W+P treatment, attaining the bottom of the ranking with a cumulative score of 10 (out of 24).

4. Discussion

Identifying grasses exhibiting drought and nutrient scarcity tolerance will aid in the production of breed forage varieties which are better adapted to climate change [49,50]. In this regard, despite the high potential of bromegrass for producing high-quality forage in temperate regions, little attention has been paid to selecting more efficient genotypes in regards to water and nutrient use [51]. The main studies assessing the PUE and/or its components (PUPE or PUTE) have only been carried out using traditional crops such as cereals, legumes, and potatoes [20,45,52]. In the case of bromegrass, most of the research has focused on the ability of this specie to cope with a single stress, mainly drought [53,54,55,56], or on evaluating their response to P and N fertilization [35,38]. Nevertheless, the effect of P and water restriction on brome development has not yet been assayed. This manuscript presents the first investigation of the response of Bromus species to the combined effects of phosphorus (P) deficiency and water deficit stress. These adverse conditions are frequently encountered in field environments, and our aim is to simulate the challenges faced by these species in their natural habitats and agricultural settings, where resources are often scarce.
The five Bromus genotypes used in this study belong to four species and were collected from different geographical areas (Table 1). Thus, each possessed a very different genetic background and exhibited a phenotypic variability to water and P deprivation ikn regards to plant growth, P uptake, and dry biomass production (Figure 2, Figures S1 and S2, Supplementary Materials).
It has been well documented that P and/or water scarcity cause a decrease in photosynthesis, carbohydrate synthesis, cell division, and elongation, thereby adversely affecting plant growth and development [13,57,58,59,60]. These adverse effects reduced plant growth in all species exposed to P scarcity, a condition which is further exacerbated by water deprivation (Figure 2 and Table S2).
Several reports indicated that bromegrasses are tolerant of water deficit stress [30,32,40,54,56,61,62]. Our results support the ability of this species to adapt to water stress conditions in the early plant growth stages, with high root growth as one adaptative plant strategy that could explain its good performance [63]. Previously, López et al. [40] declared that one plant adaptative mechanism of B. valdivianus to cope with water deficit stress is reducing its shoot ratio. Our results corroborate this observation (Figure 2), which was evidenced in all of the Bromus species studied, as both phosphorus and water affected the shoot:root ratio, regardless of the genotype (Table S1). Furthermore, the response of Bromus and L. perenne to water and P deficit stress was quite different. For example, the bromegrasses promoted root growth under P and water scarcity (−W−P), probably to the detriment of shoot growth. On the contrary, L. perenne (Nui) exhibited a high shoot growth but little root development (high shoot: root ratio, Figure 2A) under the same conditions. However, without water and P limitations (+W+P), Nui showed a higher root growth than did the bromegrass (Figure 2D), which is in agreement with previous studies that compared the performance of B. valdivianus and L. perenne when faced with water deficit stress [32,40].
On the other hand, differences in shoot dry matter production were observed among the species, especially in regards to the shoot growth rate (assessed by each cut, Figure S1). The shoot dry matter production of L. perenne was much higher than that of bromegrass in all the treatments, but only until the third cut. After that, it began to abruptly decline, whereas the bromegrasses showed little or no decline. The decrease in soil volumetric humidity was observed for the −W treatments, as well as with the increase in the frequency of irrigations in the +W treatments (Figure 1), suggesting that after the third cut, L. perenne lost more water, probably due to a higher rate of shoot biomass production, along with changes in the environmental conditions (higher temperatures), which promoted higher evapotranspiration. Under the abovementioned conditions, the bromegrasses were more tolerant than the ryegrass, especially for stressed scenarios (Figure 2 and Figure S1). Similar results were observed previously by Okamoto et al. [64] in a pot experiment conducted under drought conditions, who reported that Bromus inermis, a related species, was more tolerant than L. perenne to water deficit stress. In addition, Descalzi et al. [39] reported that under water deficit stress, the biomass production of L. perenne was more affected than that of the B. valdivianus. The ability of bromegrass to produce more dry matter during water deficit scarcity was also noted by Ordoñez et al. [32]. Nevertheless, all of the authors reported that when optimum water irrigation was applied, the tiller production and the number of shoots per plant of L. perenne were higher than those of the Bromus samples, observations which are in agreement with our findings (Figure S1).
Moreover, the Brome genotypes showed a significant variation in their ability to use water and P under low and high levels of both components (Table 3 and Table S2, Figure 2, Figure 3 and Figure S1), which allows for the categorization of P-efficient genotypes for PUE and/or WUE [47,65].
The best performance for PUE and WUE in all imposed conditions was obtained by genotype 3457 (total score 20 out of 24, Table S3), which performed better under P deprivation, enhancing the PUPE, which resulting in its high ranking (Figure 4 and Figure 5). According to Malhotra et al. [66], genotypes with a high PUE tend to have a higher root biomass under P scarcity, which can result in a better acquisition of nutrients and water. However, no differences in root biomass production were observed in the −P treatment in our study. We hypothesize that the root architecture and the rate of root formation may be related to the good results obtained by 3457 (Figure 2). It has been shown that nutrient deficiency induces changes in the architecture, morphology, and root growth rate [67,68]. Although we did not measure these parameters in this study, the rapid development of shoot growth during the first cut in the 3457 genotype (Table S2 in the Supplementary Material) could indicate a rapid root development, but further studies are needed to evaluate this hypothesis.
On the other hand, the top three positions in the PUE and WUE (Table S3) rankings of the bromegrass genotypes were obtained by advanced lines from the Agricultural Research Institute (INIA) breeding program. This may indicate that the selection and breeding for higher dry matter yield may have indirectly increased nutrient and water efficiency, as previously reported in more traditional crops such as wheat [5,69].
The genotype Pro 94-49 (B. Lithobius) earned the bottom position for PUE and WUE in all the conditions evaluated (Table S3). A previous study evaluated the performance of different genotypes of B. stamineus and B. litobius (including Pro 94-49) in response to increase in aluminum concentrations. Genotype 94-49 showed the highest root development among the group, along with the highest tolerance to elevated concentrations of Al. Marschner [70] suggests that Al tolerance and P acquisition are often interrelated. However, our work did not support that finding because Pro94-49 exhibited the lowest root development and the lowest efficiency for both P and water use (Figure 2 and Figure S1). Therefore, further studies are required to elucidate the performance of this genotype when faced with P and water scarcity.
Finally, a good performance in terms of PUE and WUE was observed for L. perenne, especially during the first three cuts. From cut number 4 onwards, there was a drop in dry matter production and, therefore, in P uptake as well, which affected both PUE and WUE (Figure S1). The superiority of L perenne could be related to the high domestication of this species, which began in the 17th century [50]. Some works have proposed that the domestication of species like wheat and corn has affected traits such as root architecture, improving their efficiency in both the uptake and use of phosphorus and water from the soil [71,72]. On the contrary, the domestication process for Bromus is relatively incipient [51], and the species is still considered by several authors to be wild and/or invasive [36,73]. It is imperative to focus on selecting and improving this species as an alternative for forage production during water scarcity. In addition, it is essential to elucidate and measure the plant’s adaptive strategies for both phosphorus and water acquisition.

5. Conclusions

As far as we know, this is the first study evaluating the combined effect of the limitation of both P and irrigation on P and water use efficiency in bromegrass genotypes. Our results showed that phosphorus and water limitation adversely affected the growth traits, the shoot and root phosphorus accumulation, and the dry matter production of brome. Our results demonstrated the ability of Bromus species to withstand the stress of water deficit, which was already evident at the early stages of growth. Such plant adaptation strategies showed a genetic variability among the Bromus genotypes, related mainly to the root growth of this species under P and water deficit conditions, which were different from those shown by perennial ryegrass.
A high genetic variability in regards to phosphorus and water use efficiency was also observed among Bromus genotypes. The 3457 genotype was the most efficient in terms of phosphorus and water use efficiency, especially under conditions of P scarcity. The genotypes 3287 and 3771, along with the cultivar Bronco, were mainly classified as “medium” for PUE and WUE, achieving a score of 16 out of 20. The genotype Pro 94-49A was inefficient under most conditions; it did not respond to phosphorus and water additions.
Categorizing genotypes according to phosphorus and water use efficiency would allow breeders to select and subsequently develop new cultivars adapted to various agroecological conditions related to water and phosphorus availability. However, to obtain the best candidates for inclusion in breeding programs, further studies are needed to evaluate the adaptation strategies of Bromus, particularly in the field and over the long term.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14010121/s1, Table S1: F-values for the main effects and factor interactions of various variables for Bromus genotypes; Table S2: Shoot and root P concentrations of five Bromus genotypes and one L. perenne cultivar (Nui), evaluated under two irrigation conditions and two P concentrations; Table S3: Categorization of Bromus genotypes for phosphorus use efficiency (PUE) and water use efficiency (WUE) based on their index score; Figure S1: Shoot dry matter production, phosphorus use efficiency (PUE), and water use efficiency (WUE) of each individual cut; Figure S2: Shoot P uptake of each individual cut (six in total) and root P uptake.

Author Contributions

Conceptualization, S.M. and A.M.; methodology, S.M., F.O.-K., R.L.-O. and P.M.d.S.C.; formal analysis, S.M. and H.A.; investigation, P.C. (Pamela Cea); resources, F.O.-K.; data curation, S.M. and R.P.-M.; writing—original draft preparation, S.M. and R.P.-M.; writing—review and editing, S.M., N.K., G.O. and A.S.; funding acquisition, S.M., P.C. (Paula Cartes) and A.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by ANID through the FONDECYT project, numbers 1220190, 1201257, and 1211387, granted to S.M., P.C. (Paula Cartes) and A.S., respectively; and by the Subsecretaría de Agricultura, Gobierno de Chile, Programa de Recursos Genéticos, number 30-501453-70, granted to P.M.d.S.C.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Variation in volumetric soil humidity during the bromegrasses growth experiment. +W = well-watered; −W = water-stressed; IT = irrigation threshold; FC = field capacity; WP = wilting point.
Figure 1. Variation in volumetric soil humidity during the bromegrasses growth experiment. +W = well-watered; −W = water-stressed; IT = irrigation threshold; FC = field capacity; WP = wilting point.
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Figure 2. Dry matter * production of shoots (sum of six cuts) and roots (after the final cut of shoots) of five Bromus genotypes and one L. perenne cv. (Nui), evaluated under two irrigation conditions (well-watered, +W; water-stressed, −W= 30% of the water applied to +W) and two P concentrations (−P: 4 mg P kg−1 and +P: 30 mg P kg−1). Each value represents the mean ± standard error. Tukey’s multiple range tests were performed only on the Bromus genotypes, whereas L. perenne was used only as a reference; different letters among columns indicate a significant difference at p ≤ 0.05. (A) water-stressed and low P; (B) well-watered and low P; (C) water-stressed and high P; (D) well-watered and high P. (*) The dry matter production of each individual cut is shown in Figure S1, Supplementary Materials.
Figure 2. Dry matter * production of shoots (sum of six cuts) and roots (after the final cut of shoots) of five Bromus genotypes and one L. perenne cv. (Nui), evaluated under two irrigation conditions (well-watered, +W; water-stressed, −W= 30% of the water applied to +W) and two P concentrations (−P: 4 mg P kg−1 and +P: 30 mg P kg−1). Each value represents the mean ± standard error. Tukey’s multiple range tests were performed only on the Bromus genotypes, whereas L. perenne was used only as a reference; different letters among columns indicate a significant difference at p ≤ 0.05. (A) water-stressed and low P; (B) well-watered and low P; (C) water-stressed and high P; (D) well-watered and high P. (*) The dry matter production of each individual cut is shown in Figure S1, Supplementary Materials.
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Figure 3. Means for phosphorus use efficiency (PUE) and water use efficiency (WUE) of five Bromus genotypes, evaluated under two irrigation conditions (well-watered, +W; water-stressed, −W= 30% of the water applied to +W) and two P concentrations (−P: 4 mg P kg−1 and +P: 30 mg P kg−1). Different letters within a scenario indicate a significant difference at p ≤ 0.05, according Tukey’s multiple range tests.
Figure 3. Means for phosphorus use efficiency (PUE) and water use efficiency (WUE) of five Bromus genotypes, evaluated under two irrigation conditions (well-watered, +W; water-stressed, −W= 30% of the water applied to +W) and two P concentrations (−P: 4 mg P kg−1 and +P: 30 mg P kg−1). Different letters within a scenario indicate a significant difference at p ≤ 0.05, according Tukey’s multiple range tests.
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Figure 4. Phosphorus use efficiency (PUE) of five Bromus genotypes and one L. perenne cultivar (Nui) identified as efficient (E = 3 points), medium (M = 2 points), and inefficient (I = 1 point), evaluated at two irrigation conditions (well-watered, +W and water-stressed, −W = 30% of water applied to +W) and two P concentrations (Low P: −P = 4 mg P kg−1 and High P: +P = 30 mg P kg−1). (A) water-stressed and low P; (B) well-watered and low P; (C) water-stressed and high P; (D) well-watered and high P.
Figure 4. Phosphorus use efficiency (PUE) of five Bromus genotypes and one L. perenne cultivar (Nui) identified as efficient (E = 3 points), medium (M = 2 points), and inefficient (I = 1 point), evaluated at two irrigation conditions (well-watered, +W and water-stressed, −W = 30% of water applied to +W) and two P concentrations (Low P: −P = 4 mg P kg−1 and High P: +P = 30 mg P kg−1). (A) water-stressed and low P; (B) well-watered and low P; (C) water-stressed and high P; (D) well-watered and high P.
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Figure 5. Water use efficiency (PUE) of five Bromus genotypes and one L. perenne cultivar (Nui) identified as efficient (E = 3 points), medium (M = 2 points), and inefficient (I = 1 point), evaluated at two irrigation conditions (well-watered, +W, and water-stressed, −W = 30% of water applied to +W) and two P concentrations (Low P: −P = 4 mg P kg−1 and High P: +P = 30 mg P kg−1). (A) water-stressed and low P; (B) well-watered and low P; (C) water-stressed and high P; (D) well-watered and high P.
Figure 5. Water use efficiency (PUE) of five Bromus genotypes and one L. perenne cultivar (Nui) identified as efficient (E = 3 points), medium (M = 2 points), and inefficient (I = 1 point), evaluated at two irrigation conditions (well-watered, +W, and water-stressed, −W = 30% of water applied to +W) and two P concentrations (Low P: −P = 4 mg P kg−1 and High P: +P = 30 mg P kg−1). (A) water-stressed and low P; (B) well-watered and low P; (C) water-stressed and high P; (D) well-watered and high P.
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Table 1. Identification and origin of bromegrass genotypes used in the study.
Table 1. Identification and origin of bromegrass genotypes used in the study.
GenotypeGenusSpeciesCollection SiteCoordinatesYear of Collection
Line 3287BromusvaldivianusCollipulli, Chile−38,01; −72,211992
Line 3457BromuscoloratusLlanquihue, Chile−41,13; −73,031992
Line 3771BromuscoloratusVillarrica, Chile−30,05; −72,241992
cv. BroncoBromusvaldivianus---------------
Line PRO 94-49 ABromuslithobiusQuillén, Argentine−39,58; −71,451994
cv. NuiLoliumperenne----------------
Table 2. Chemical and physical analyses of the soil.
Table 2. Chemical and physical analyses of the soil.
ParameterValue
pH (water)6.08
pH (CaCl2)5.54
Organic matter (%)25.2
N (mg kg−1)15
P (mg kg−1)4.01
K (mg kg−1)150.1
Ca (cmol (+) kg−1)6.06
K (cmol (+) kg−1)0.38
Mg (cmol (+) kg−1)1.55
Na (cmol (+) kg−1)0.08
Al (cmol (+) kg−1)0.06
CICE (cmol (+) kg−1)8.14
Saturation of Al (%)0.75
B (mg kg−1)0.22
S (mg kg−1)16.62
Zn (mg kg−1)1.82
Mn (mg kg−1)15.37
Cu (mg kg−1)14.27
Fe (mg kg−1)198.7
Sand (%)20.1
Silt (%)55.4
Clay (%)24.5
Textural classification Silty loam
Field capacity (1/3 atm) (%wt/wt)76.83
Permanent wilting point (15 atm) (%wt/wt)50.61
Humidity retention (1/3–15 atm) (%wt/wt)26.22
Bulk density0.765
Table 3. Phosphorus uptake efficiency (PUPE) and phosphorus utilization efficiency (PUTE) of five Bromus genotypes and one L. perenne cv. (Nui), evaluated under two irrigation conditions (well-watered, +W; water-stressed, −W = 30% of the water applied to +W) and two P concentrations (−P: 4 mg P kg−1 and +P: 30 mg P kg−1). Each value represents the mean ± standard error. Tukey’s multiple range tests were only performed on the Bromus genotypes, whereas L. perenne was used only as a reference; different letters within a column indicate a significant difference at p ≤ 0.05.
Table 3. Phosphorus uptake efficiency (PUPE) and phosphorus utilization efficiency (PUTE) of five Bromus genotypes and one L. perenne cv. (Nui), evaluated under two irrigation conditions (well-watered, +W; water-stressed, −W = 30% of the water applied to +W) and two P concentrations (−P: 4 mg P kg−1 and +P: 30 mg P kg−1). Each value represents the mean ± standard error. Tukey’s multiple range tests were only performed on the Bromus genotypes, whereas L. perenne was used only as a reference; different letters within a column indicate a significant difference at p ≤ 0.05.
GenotypePUPE (g P Uptake g−1 P Supply)PUTE (g DW g−1 P Uptake)
−W+W−W+W
−P+P−P+P−P+P−P+P
Line 32871.39 ± 0.21 bc0.53 ± 0.01 b3.52 ± 0.28 ab1.22 ± 0.1 a374 ± 42.13 a249 ± 3.12 a361 ± 0.92 ab230 ± 27.71 a
Line 34571.98 ± 0.22 a0.71 ± 0.11 a4.31 ± 0.26 a1.21 ± 0.19 a328 ± 25.69 a214 ± 26.69 ab340 ± 28.11 ab249 ± 33.07 a
Line 37711.73 ± 0.14 ab0.64 ± 0.07 ab3.6 ± 0.42 ab1.19 ± 0.15 a328 ± 4.72 a246 ± 15.06 a324 ± 21.17 b243 ± 30.34 a
Bronco1.64 ± 0.18 abc0.72 ± 0.03 a3.06 ± 0.58 b1.41 ± 0.07 a316 ± 8.45 a217 ± 6.13 ab401 ± 43.64 a221 ± 13.11 a
Pro94-49 A1.15 ± 0.09 c0.6 ± 0.04 ab3.2 ± 0.43 ab1.28 ± 0.07 a334 ± 30.81 a203 ± 9.1 b324 ± 17.58 ab216 ± 4.66 a
Nui2.24 ± 0.230.99 ± 0.084.76 ± 0.911.43 ± 0.03307 ± 18.61187 ± 13.61293 ± 46.41205 ± 8.45
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Meier, S.; de Souza Campos, P.M.; Morales, A.; López-Olivari, R.; Ortega-Klose, F.; Aponte, H.; Cartes, P.; Khan, N.; Ondrasek, G.; Cea, P.; et al. Evaluation and Selection of Bromegrass Genotypes under Phosphorus and Water Scarcity towards the Development of Resilient Agriculture Focusing on Efficient Resource Use. Agronomy 2024, 14, 121. https://doi.org/10.3390/agronomy14010121

AMA Style

Meier S, de Souza Campos PM, Morales A, López-Olivari R, Ortega-Klose F, Aponte H, Cartes P, Khan N, Ondrasek G, Cea P, et al. Evaluation and Selection of Bromegrass Genotypes under Phosphorus and Water Scarcity towards the Development of Resilient Agriculture Focusing on Efficient Resource Use. Agronomy. 2024; 14(1):121. https://doi.org/10.3390/agronomy14010121

Chicago/Turabian Style

Meier, Sebastián, Pedro M. de Souza Campos, Arturo Morales, Rafael López-Olivari, Fernando Ortega-Klose, Humberto Aponte, Paula Cartes, Naser Khan, Gabrijel Ondrasek, Pamela Cea, and et al. 2024. "Evaluation and Selection of Bromegrass Genotypes under Phosphorus and Water Scarcity towards the Development of Resilient Agriculture Focusing on Efficient Resource Use" Agronomy 14, no. 1: 121. https://doi.org/10.3390/agronomy14010121

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