EFFECT OF SOLUTION NITROGEN CONCENTRATION ON YIELD ...

JOURNAL OF PLANT NUTRITION, 25(2), 245–258 (2002)

EFFECT OF SOLUTION NITROGEN CONCENTRATION ON YIELD, LEAF ELEMENT CONTENT, AND WATER AND NITROGEN USE EFFICIENCY OF THREE HYDROPONICALLY-GROWN ROCKET SALAD GENOTYPES Pietro Santamaria,1,* Antonio Elia,2 and Francesco Serio2 1

Dipartimento di Scienze delle Produzioni Vegetali, University of Bari, Via Amendola, 165/A, Bari 70126, Italy 2 Istituto sull’Orticoltura Industriale, CNR, Via Amendola, 165/A, Bari 70126, Italy

ABSTRACT Two species of rocket salad, Eruca vesicaria L. subsp. sativa Miller and Diplotaxis tenuifolia L. DC, were grown hydroponically in a growth chamber with two nitrogen levels (1 or 8 mM N) to evaluate nitrate accumulation and nitrogen use efficiency. One ecotype of Eruca and two of Diplotaxis were used. Nitrogen (N) increased leaf production and the contribution of leaves to the total dry mass production in E. vesicaria but not in D. tenuifolia, and emphasized leaf area differences between the

*Corresponding author. E-mail: [email protected] 245 Copyright # 2002 by Marcel Dekker, Inc.

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two species. The two species also showed differences in the inorganic anions and N content. D. tenuifolia ecotypes accumulated more NO3 than E. vesicaria (7.7 vs. 4.7 g kg 1 fresh mass). By increasing N concentration in the nutrient solution, NO3 content in leaves expressed on fresh mass basis increased in both species by 52%. Nitrogen use efficiency was greater in E. vesicaria than in D. tenuifolia (19.0 vs. 18.0), and decreased with increasing nitrogen in the nutrient solution (19.0 vs. 17.6).

INTRODUCTION Rocket salad is a leafy vegetable popular in the Mediterranean region. The popularity of rocket salad as a food crop is due to its spicy hot flavor and is used as garnish to salads, snacks, and a wide variety of meals (1). Recently, rocket salad has gained Northern European markets where salads have a great importance in meal composition, which proves the growing interest of consumers and producers. Indeed, rocket salad cultivation has widened to also include soilless systems (2). Also for rocket, as for other Italian export vegetables (e.g. lettuce, spinach, and potato), sales contracts include very strict clauses, such as with Switzerland and Germany. Namely, nitrate content for rocket is required not to exceed 2.5– 4.0 g kg 1 of fresh mass, which is a very strict threshold difficult to respect because of the high accumulation of nitrates (NO3) in rocket, even when reduced amounts of nitrate in the cultivation means are used (3). In rocket, two recent surveys carried out in Italy show NO3 content reaches up to 9,300 mg kg 1 of fresh product (4,5). Nitrate has a low toxicity to humans. Products of nitrate reduction, however, are toxic and can lead to severe pathologies in humans. These products include nitrite alone or the nitroso-N compounds that form when nitrite binds to other substances before or after ingestion. Therefore, the presence of nitrate in vegetables, drinking water, and generally in food is a public health issue (6). The importance of nitrate content in vegetables is underlined in the European Commission Regulations No. 194/97 and 864/99 [Commission Regulation (EC) n. 194/97, published in the Official Journal of the European Communities L31/48 of February 1 1997; Commission Regulation (EC) n. 864/99, published in the Official Journal of the European Communities L108/16 of 26 April 1999], setting the maximum nitrate levels in the different seasons and cultivation methods for lettuce and spinach. For lettuce limits are: 4.5 g kg 1 of fresh mass (f.m.) from 1/10 to 31/3 and 3.5 g kg 1 f.m. from 1/4 to 30/9; only for open field cultivated lettuce harvested

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from 1/5 to 31/8 NO3 content must not be above 2.5 g kg 1 f.m. (in the absence of appropriate labeling indicating the production method, the limit established for open-grown lettuce applies). Under the name of rocket salad a number of species of the Brassicaceae family are grouped belonging to the Eruca Miller and Diplotaxis DC genera. Eruca is present in both wild and cultivated forms; Diplotaxis is known as a wild type. In both cases, genetic improvement activities are still scarce and there are neither selected populations nor cultivars. The present research aims to study nitrate accumulation and nitrogen use efficiency of different genotypes of rocket salad grown with two nitrogen levels.

MATERIALS AND METHODS Trials involved two species of rocket salad, Eruca vesicaria L. subsp. sativa Miller (cv. Coltivata – Royal Sluis, Mirandola, Italy) and Diplotaxis tenuifolia (L.) DC. Two ecotypes of this latter were used; one was locally produced at Bari (D.t. 1) and the other (D.t. 2) is available on the market (Olter, Asti, Italy). Seeds were germinated in seedling trays filled with a 3:2:1 v/v/v mixture of peat, vermiculite, and perlite in a growth chamber (model Conviron PGW36, with useful surface of 3.3 m2 and useful maximum height of 2 m). The following weather parameters were set: photoperiod (day/night hours) 12/12, relative humidity not below 65%, temperature 18/15 C, and irradiance 240 mmol m 2 s 1 of photosynthetically active photon flow (PPF) [measured at the center of the growth chamber and above leaves, with quantum sensor Licor LI-190 SA connected to Licor Quantum instrument Model LI-189 (Lincoln, NE)]. Germination took place after 7 days for E. vesicaria and after 8 and 12 days for D.t. 1 ecotype and for D.t. 2 wild rocket salad, respectively. After emergence, in order to promote root growth, the boxed containers were left floating in glass vessels containing a nutrient solution with nitrate nitrogen only, with nutrient concentration at 50% of that suggested by Hoagland and Arnon (7). Plants were kept in these conditions to the phenological stage of 4–5th true leaf. Nineteen, 26, and 29 days after emergence of E. vesicaria, the D.t. 1, and the D.t. 2 wild rocket salad, respectively, plants were transferred, after thorough removal of the substrate from roots, and grown soilless in holes on lids of trunk-conic plastic pots containing about 7 L tap water (5 plants per pot). Plants were kept in this solution one day to allow complete removal of substrate residues and plant adaptation to the growth system. Later, water was replaced with a solution of 1 mM N (Table 1), in which plants were kept for 7 more days.

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Table 1. Composition of Nutrient Solutions for Two Different N Levels (Micronutrients Were Applied According to Hoagland and Arnon 1950) Compound (mM) N (mM) 1 8

HNO3

Ca(NO3)2

KNO3

CaCl2

K2SO4

H3PO4

0.6 0.6

0 1.7

0.4 4.0

1.7 0

1.8 0

1.0 1.0

Starting from the stage of 6–7th true leaf, nitrogen treatments applied were different using 2 levels of N (1 and 8 mM). Table 1 reports the compounds used to obtain the set concentrations of all elements [phosphorus (P), potassium (K), calcium (Ca), and magnesium (Mg) at 31, 160, 132, and 15 mg L 1, respectively], starting from tap water which contained 17, 3.6, 10, 11, 2.6, 15, and 64 mg L 1 of chloride (Cl), NO3-N, SO4-sulfur (S), sodium (Na), K, Mg, and Ca, respectively. A completely randomized experimental design with three replications (pots) was used. Air was continuously bubbled through pots to supply oxygen. All solutions were renewed ex-novo every 3–5 days and pH (5.5–6.5) was maintained by addition of HCl or NaOH 0.5 N twice a day. At each change of the nutrient solutions, residual and fresh nutrient solution in each pot was weighed to assess water uptake by the plant. From the application of different nitrogen treatments, trials lasted 12 days for D. tenuifolia and 10 days for E. vesicaria. At harvest, leaf number, fresh mass, and area (by LI-3100 leaf area meter; LI-COR, Lincoln, NE) were determined, together with root fresh mass and length. All plant material was dried in a thermo-ventilated oven at 65 C until reaching a constant mass. After assessment of dry mass, plant samples were submitted to quantitative chemical analysis of Cl, NO3, SO4, H2PO4, and total N. Inorganic anions were determined in aqueous extracts from 0.5 g dry plant material using an Ion Chromatograph (Dionex DX500, Dionex Corp., Sunnyvale, CA) with the AS4A column (5). Total N of leaves and roots was determined with Kjeldahl method (by Kjeltec 2300 auto analyzer, Foss-Tecator, Hillerød, Denmark) by adding salicylic acid to recover NO3-N. On account of these basic data, water use efficiency (WUE) was calculated by comparing biomass production to consumed nutrient solution (supposed as equal to transpired water); nitrogen use efficiency (NUE) was calculated as a ratio between biomass production and accumulated nitrogen; reduced nitrogen as the difference between total N and NO3-N.

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Data were subjected to SAS’s (Cary, NC) general linear model procedure. On account of the research goals, orthogonal contrasts were inferred with a single freedom level to compare E. vesicaria vs. D. tenuifolia and the ecotypes of D. tenuifolia between them. To study linear and quadratic trends of daily uptake of nutrient solution as a function of growth days, polynomial contrasts were examined starting from measures taken at changes of nutrient solution 3, 7, and 10 days after beginning of treatments for E. vesicaria and 3, 7, and 12 days after the beginning of treatments for the two ecotypes of D. tenuifolia. Only significant differences obtained from variance analysis ( p < 0.05) are presented. RESULTS Yield and Morphological Features D. tenuifolia plants formed more leaves than E. vesicaria (14.5 vs. 10), but fresh mass and leaf area were lower in the former than in the latter (Table 2). By increasing N concentration from 1 to 8 mM, leaf fresh weight increased by 15% in D. tenuifolia and by 47% in E. vesicaria (Table 3); consistently, leaf area increased by 9% in the former and by 38% in the latter (figure not shown). Dry matter content of D. tenuifolia leaves was 6 g kg 1 of fresh mass greater than that of E. vesicaria (Table 2). Fresh mass and root length of E. vesicaria were higher than D. tenuifolia ecotypes; between these latter, D.t. 2 showed higher fresh mass and root length (Table 2). On average, root dry matter content of D. tenuifolia was higher than that of E. vesicaria (Table 2); between D. tenuifolia ecotypes the highest root dry matter content was recorded for D.t. 1, which exceeded by 21 g kg 1 of fresh mass the other ecotype (Table 2). Leaf contribution to the whole plant dry mass increased with increasing N more in cultivated than in wild rocket salad (Table 3).

Leaf Content of the Main Inorganic Anions By increasing N concentration in the nutrient solution from 1 to 8 mM, NO3 content in leaves increased by 59 and 52% expressed on dry or fresh mass basis, respectively, and resulted to be on average 58% higher in D. tenuifolia than in E. vesicaria (Table 4). With 8 mM of N, Cl and H2PO4 reached 50% and 83% concentrations, respectively, compared to their concentrations with 1 mM (Table 4). E. vesicaria

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Table 2. Yield and Morphological Characteristics of Rocket Plants as Affected by N Level in the Nutrient Solution and Rocket Genotype Leaf

Root

Fresh Dry Fresh Dry Number Mass Area Mass Mass Mass Length (n) (g) (cm2) (g kg 1 f.m.) (g) (g kg 1 f.m.) (cm) N (mM) 1 8 Genotypea D. tenuifolia 1 D. tenuifolia 2 E. vesicaria Significanceb N Genotype Dipl. vs. Eruca D.t. 1 vs. D.t. 2 N* Genotype N*(Dipl. vs. Eruca) N*(D.t. 1 vs. D.t. 2)

12 13

5.6 113 7.4 142

90 88

3.0 3.4

72 70

29.6 29.6

14 15 10

3.8 80 4.8 78 10.8 224

92 90 85

1.7 2.6 5.2

86 65 62

22.3 26.9 39.5

NS *** *** NS NS NS NS

* *** *** NS * * NS

NS * ** NS NS NS NS

NS *** *** * NS NS NS

NS ** * ** NS NS NS

NS *** *** * NS NS NS

* *** *** NS * * NS

a

D. tenuifolia 1: locally produced ecotype (Bari); D. tenuifolia 2: ecotype from ‘Olter’ seed company. b NS, *, **, ***, Nonsignificant or significant at p < 0.05, < 0.01, and < 0.001, respectively. Interactions, if significant, are reported in Table 3.

Table 3. Interaction Effect N*(Diplotaxis tenuifolia vs. Eruca vesicaria subsp. sativa) (P < 0.05) on Fresh and Dry Weight, Sulfate Content of Leaves and Water Use Efficiency in Rocket Plants Genotype D. tenuifolia E. vesicaria a

SO4 N Level Leaf Fresh Weight Leaf Dry Weight WUE (mM) (g) (g kg 1 d.m.)a (g kg 1 d.m.) (g L 1) 1 8 1 8

4.0 4.6 8.8 12.9

c c b a

701 723 715 765

b b b a

42 35 64 41

b c a b

2.6 2.3 2.7 3.7

b b b a

Grams of dry matter leaves weight per 1000 g of total plant dry matter weight. Within each cloumn, values followed by the same letters are not significantly different.

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Table 4. Main Inorganic Anions Leaf Content of Rocket Plants as Affected by N Level in the Nutrient Solution and Rocket Genotype Cl

NO3 (g kg

N (mM) 1 8 Genotypea D. tenuifolia 1 D. tenuifolia 2 E. vesicaria Significanceb N Genotype Diplotaxis vs. Eruca D. tenuifolia 1 vs. 2 N* Genotype N*(Dipl. vs. Eruca) N*(D.t. 1 vs. D.t. 2)

H2PO4 1

SO4 NO3 (g kg 1 f.m.)

d.m.)

18 9

58 92

18 15

50 37

5.3 8.1

14 12 15

87 83 55

10 19 20

34 43 53

8.0 7.3 4.7

*** * * * NS NS *

*** *** *** NS NS NS NS

* *** *** *** NS NS NS

*** *** *** * * * NS

*** *** *** NS NS NS NS

a

D. tenuifolia 1: locally produced ecotype (Bari); D. tenuifolia 2: ecotype from ‘Olter’ seed company. b NS, *, ***, Nonsignificant or significant at p < 0.05 and < 0.001, respectively. Interactions, if significant, are reported in Table 3.

accumulated 2, 5, and 15 g kg 1 of dry mass more of Cl, H2PO4 and SO4, respectively, than D. tenuifolia ecotypes (Table 4). The D.t. 1 ecotype accumulated more Cl and less H2PO4 and SO4 than D.t. 2 rocket salad (Table 4); however, difference in Cl was due to the different behavior of the two genotypes grown with 1 mM of N (Fig. 1a). By increasing N concentration in the nutrient solution from 1 to 8 mM, SO4 concentration decreased by 36 and 17% in E. vesicaria and D. tenuifolia, respectively (Table 3). Total and Reduced Nitrogen With the increase of N availability in the nutrient solution from 1 to 8 mM, total N concentration rose by 10% in leaves and by 4.3% in roots. Reduced N decreased on average by 110 g kg 1 of total N (Table 5). D. tenuifolia leaves recorded 6% more total N than E. vesicaria, but reduced N for the whole plant was 13% lower (Table 5).

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Figure 1. Effect of N level on Cl leaf content (la) (g kg 1 d.m.) and the daily water consumption (1b) (mL plant 1) in the two ecotypes of D. tenuifolia.

Table 5. Total N Content, Reduced N Fraction and Nitrogen Use Efficiency (NUE) in Rocket Plants as Affected by N Level in Nutrient Solution and Rocket Genotype N Leaves (g kg N (mM) 1 8 Genotypea D. tenuifolia 1 D. tenuifolia 2 E. vesicaria Significanceb N Genotype Diplotaxis vs. Eruca D. tenuifolia 1 vs. 2 N* Genotype N*(Dipl. vs. Eruca) N*(D.t. 1 vs. D.t. 2) a

NUE Roots d.m.)

Reduced N (g kg 1 total N)

Total

Leaves (g g 1)

Roots

55 60

47 49

763 653

19.0 17.6

18.3 16.8

21.1 20.3

59 58 55

49 48 48

669 682 774

17.9 18.0 19.0

17.0 17.1 18.4

20.5 20.8 20.9

*** ** ** NS NS NS NS

** NS NS NS NS NS NS

*** *** *** NS NS NS NS

*** ** ** NS NS NS NS

*** ** *** NS NS NS NS

** NS NS NS NS NS NS

1

D. tenuifolia 1: locally produced ecotype (Bari); D. tenuifolia 2: ecotype from ‘Olter’ seed company. b NS, **, ***, Nonsignificant or significant at p < 0.01 and < 0.001, respectively.

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Nitrogen Use Efficiency Nitrogen use efficiency (NUE) obtained with 1 mM N was 8% greater than with 8 mM N. In E. vesicaria it was 6% higher than in D. tenuifolia (Table 5). Differences were observed between the two nutrient solutions both in leaves and roots, whereas differences between genotypes only affected leaves (Table 5).

Water Uptake and Use Efficiency Total water consumption increased by 18% with increasing N availability in the nutrient solution from 1 to 8 mM; namely it was 67% higher in E. vesicaria than in D. tenuifolia (Table 6). In E. vesicaria, average daily uptake rose from 17.4 to 35.0 mL plant 1 with 1 mM N and from 16.9 to 41.8 mL plant 1 with 8 mM N, 3 and 10 days, respectively, from the beginning of treatments (Fig. 2). Daily average uptake of D.t. 1 rocket salad remained almost constant and was not affected by N,

Table 6. Water Consumption and Water Use Efficiency (WUE) in Rocket Plants as Affected by N Level in Nutrient Solution and Rocket Genotype Water Consumption (mL) N (mM) 1 8 Genotypea D. tenuifolia 1 D. tenuifolia 2 E. vesicaria Significanceb N Genotype Diplotaxis vs. Eruca D. tenuifolia 1 vs. 2 N* Genotype N*(Dipl. vs. Eruca) N*(D.t. 1 vs. D.t. 2) a

WUE (g L

191 225

2.6 2.8

162 178 284

2.6 2.3 3.2

* *** *** NS NS NS NS

NS * ** NS * * NS

1

)

D. tenuifolia 1: locally produced ecotype (Bari); D. tenuifolia 2: ecotype from ‘Olter’ seed company. b NS, *, **, ***, Nonsignificant or significant at p < 0.05, < 0.01, and < 0.001, respectively. Interactions, if significant, are reported in Table 3.

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whereas it rose by 25% for D.t. 2 ecotype when N was increased from 1 mM to 8 mM (Fig. 1b). Water use efficiency (WUE) in E. vesicaria was greater than in D. tenuifolia when 8 mM N was used, but not with 1 mM N (Table 3).

DISCUSSION The three genotypes under study showed different behavior starting in the early cultivation stages. Seed emergence in E. vesicaria was faster than in the D. tenuifolia ecotypes, and among the latter the Bari-produced ecotype emerged earlier. Later phenological stages also showed different features among the three genotypes. From emergence to IV-V true leaf formation 20, 27, and 30 days were needed for E. vesicaria, D.t. 1, and D.t. 2, respectively. Although nitrogen treatments lasted 10 days for E. vesicaria and 12 days for D. tenuifolia, and trial covered, from emergence to harvest, 30, 39, and 42 days for E. vesicaria, D.t. 1, and D.t. 2, respectively, leaf production for the first genotype doubled that of the others and was characterized by a lower number of leaves but a higher leaf area (Table 2). Nitrogen increased leaf production and the contribution of leaves to the total dry mass production in E. vesicaria, but not in D. tenuifolia (Table 6), and stressed leaf area differences between the two species.

Figure 2. Influence of nitrogen level and of the number of days from the beginning of treatment on daily water consumption in E. vesicaria.

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The two species showed differences also in the tendency for accumulation of inorganic anions and N. Noteworthy is the great capability of D. tenuifolia ecotypes to accumulate nitrate (on average 2.9 g kg 1 fresh mass more NO3 than E. vesicaria) (Table 4). In terms of hazards for public health, these data show that to outgrow the acceptable daily intake (ADI) of NO3, as established by the World Health Organization (6) for a 60 kg person, 46 to 29 g of E. vesicaria and D. tenuifolia, respectively, are sufficient (36 and 24 g would be sufficient if 8 mM N are used). However, it should be considered that JEFCA (Joint FAO/WHO Expert Committee on Food Additives) was cautious in the determination of nitrates for the ADI, since vegetables are in many respects beneficial to human health, and it would be inappropriate to compare exposure to nitrates from vegetables directly with the ADI, hence to infer nitrate limitations in vegetables simply from this one (6). The different capability of rocket salad species to accumulate nitrates could be due to the different location and activity of nitrate reductase in the plant (8), or to differences in NO3 absorption and transport from roots to leaves. The former hypothesis was put forward to explain differences found in spinach cultivars (9) and between cucumber and pea (10); the latter, instead, would explain differences observed between lettuce cultivars (11). Rocket salad can absorb NO3 very quickly (12), as confirmed in the present research results; NO3 concentration in leaves was much higher than in the nutrient solution. With 1 and 8 mM NO3-N in the nutrient solution, NO3 accumulation ratio (expressed as ratio between the concentration in leaves and in the external solution) was, respectively, 55 and 12 for E. vesicaria and 101 and 18 for D. tenuifolia. Nitrogen content was also high, and higher in D. tenuifolia than in E. vesicaria, and, obviously, increased with increasing N availability in the nutrient solution (Table 5). These results would suggest rocket salad, mainly D. tenuifolia, can be used as ‘‘cover crop’’, namely as winter species to sow after harvesting of a springsummer crop in order to remove nitrogen in soil, which would be a potential pollutant if spread in the environment (13,14). This is particularly true for areas, such as the Mediterranean ones, where rainfall is quite abundant in wintertime, exceeding evapotranspiration and soil capability to trap water. Under these conditions, a considerable portion of NO3-N can be lost through leakage and denitrification, mainly when dry summers and repeated fertilization cause high nitrogen fertilization residues in soil during the fall. The use of rocket salad, which has a short cultivation cycle, would allow an increase in the number of possible crop sequence combinations and a reduction in the environmental impact of nitrogen fertilization.

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The production and consequent harvest of 20 t ha 1 of rocket salad leaves [average yield for open field cultivation (2,15)], having similar features to those obtained in the present research work — i.e. N concentration between 5.5 and 6.0 g 100 1 dry matter (Table 5) and dry matter content of 85–90 g kg 1 of fresh product (Table 2), although dry matter percentage in leaves is higher for open field cultivation — would account for the removal of 94 –108 kg ha 1 N from soil, which is remarkable for a leafy vegetable able to complete its cycle in roughly two months. The capability to transform inorganic nitrogen into organic nitrogen (determined by subtracting NO3-N from total N) was greater in E. vesicaria than in D. tenuifolia and it decreased with increasing N availability and uptake (Table 5). Some authors consider this as luxury consumption and believe plants absorbing more nutrients than needed for growth can use this reserve to assure growth even when their availability in the cultivation substrate decreases (16,17). Nitrogen use efficiency was greater in E. vesicaria than in D. tenuifolia, and decreased with the increase of nitrogen in the nutrient solution (Table 5). NUE was rather high, even though lower than in other vegetables [23.5, 20.8, and 27.2 g of dry matter per g of N for snap bean, cucumber, and pea, respectively (18); 28 and 94 g of dry matter per g of N for pepper (19) and tomato (20) plants, respectively]. Despite the higher nitrate concentrations measured in D. tenuifolia ecotypes compared to E. vesicaria, chlorides, phosphates, and sulfates often followed an opposite trend (Table 4). The higher SO4 leaf content in E. vesicaria than in D. tenuifolia, and in D.t. 1 compared to D.t. 2 ecotype, could positively affect the spicy taste of leaves, even if with the increase of N in the nutrient solution these differences between genotypes level off (Table 3). As a consequence of the greater leaf area, E. vesicaria consumed more water than D. tenuifolia, although it used it more efficiently (Table 6), mainly when N availability in the nutrient solution was higher (Table 3).

CONCLUSIONS 1. 2. 3.

4.

There is high variability among the studied genotypes. Leaf production and leaf contribution to total plant mass increase with increasing N in the nutrient solution for E. vesicaria only. Rocket salad has a great capability to accumulate nitrates in leaves. With 8 mM N, D. tenuifolia accumulated over 9 g kg 1 of fresh product, almost 3 g kg 1 NO3 more than E. vesicaria. When N in the nutrient solution is increased, N use efficiency (NUE) decreases, though it is greater in E. vesicaria than in D. tenuifolia.

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ACKNOWLEDGMENT The University of Bari (60% 1997 fund allocation) funded the work within the Research Project ‘‘Nitrogen use efficiency and quality of leaf vegetables’’.

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18. 19. 20.

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