Ecophysiological Analysis Of Drought And Salinity Stress Of Quinoa ( Chenopodium Quinoa willd.)

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Ecophysiological Analysis Of Drought And Salinity StressOf Quinoa (Chenopodium Quinoawilld.)H. Bosque Sanchez a , R. Lemeur b , P. Van Damme b & S.-E. Jacobsen ca La Paz, Boliviab University of Ghent, Ghent, Belgiumc Quinoa Project, Lima, PeruPublished online: 18 Aug 2006.

To cite this article: H. Bosque Sanchez , R. Lemeur , P. Van Damme & S.-E. Jacobsen (2003) Ecophysiological Analysis OfDrought And Salinity Stress Of Quinoa (Chenopodium Quinoawilld.), Food Reviews International, 19:1-2, 111-119, DOI:10.1081/FRI-120018874

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Ecophysiological Analysis of Drought and Salinity Stress ofQuinoa (Chenopodium quinoa Willd.)#

H. Bosque Sanchez,1,* R. Lemeur,2 P. Van Damme,2 and S.-E. Jacobsen3

1La Paz, Bolivia2University of Ghent, Ghent, Belgium

3Quinoa Project, Lima, Peru

ABSTRACT

We assessed the relative influence of drought or salinity stress with similar soil water

potentials on growth, plant water relations, and photosynthesis rate of Chenopodium

quinoa Willd., as well as the suitability of common techniques used in stress

physiology studies. Our results from greenhouse pot experiments showed that salt

stress induced better absolute and relative growth rates, and that the plant developed

adaptation mechanisms to drought through high water use efficiency and high root

shoot ratios. The stomatal resistance and the leaf water potential increased with an

increased stress level. Variable to maximal chlorophyll fluorescence (Fv/Fm) and

quenching analysis (qP and qN) showed that dehydrated plants are less protected from

photoinhibition. The dynamic diffusion porometer is of limited use in leaves with salt

glands.

Key Words: Ecophysiology; Quinoa; Drought; Salinity; Stress.

111

DOI: 10.1081/FRI-120018874 8755-9129 (Print); 1525-6103 (Online)

Copyright q 2003 by Marcel Dekker, Inc. www.dekker.com

#Master of Science thesis. Article submitted to the First International Workshop of Quinoa. 10-14

May, 1999. Lima, Peru.*Correspondence: H. Bosque Sanchez, La Paz, Bolivia; Fax: 591-2-317050; E-mail: hbosque@

hotmail.com.

FOOD REVIEWS INTERNATIONALVol. 19, Nos. 1 & 2, pp. 111–119, 2003

MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

©2003 Marcel Dekker, Inc. All rights reserved. This material may not be used or reproduced in any form without the express written permission of Marcel Dekker, Inc.

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INTRODUCTION

Two of the most important environmental stresses influencing the productivity of

agricultural systems are drought and salinity. With the steady growth of population,

especially in developing countries, and the declining availability of new agricultural land,

the need to confront and minimize the effects of salt, drought, or any other environmental

stress on plant growth and crop yield is urgent.

The Peruvian–Bolivian Altiplano (highland plateau) at altitudes of 3000–4000 m is one

of the regions with the most severe environmental conditions for cropping. Frost and drought

are common, with high evapotranspiration rates, low relative humidity, and low dew

temperatures at night. In addition, there are high levels of UV radiation, and atmospheric CO2

pressure is about half that of sea level. The majority of the soils are marginal for farming. They

are stony, saline, and either poorly or excessively drained, and have very low natural fertility

with extreme pH values, from 4.8 in parts of Peru to 8.5 in the Bolivian salt flatlands (Fleming

and Galwey, 1995; Jacobsen, personal communication). One of the native crops well-adapted

to these harsh climatic conditions is quinoa (Chenopodium quinoa Willd). It thrives under

ecologically extreme conditions, but its physiology is still unknown. Thus, the main objective

of this investigation was to analyze the ecophysiological responses to salinity and drought

stresses of the Bolivian quinoa “Real,” determining growth parameters, stomatal resistance

(rs), leaf water potential (Cl), and chlorophyll fluorescence.

MATERIALS AND METHODS

The “Real” variety of quinoa, native to the southern Altiplano of Bolivia, was studied.

Seeds were sown in pots (10-dm3 capacity filled with loamy soil) in a greenhouse of the

Agricultural Faculty, University of Ghent, Belgium. Seedlings were thinned to three plants

per pot at the six-leaf stage. Pots were placed in a randomized complete block design with

three replications. The five treatments consisted of salinization with 3852.8 mg.L21 NaCl

(S1) and 8051.2 mg.L21 NaCl (S2), drought stress at 20.159 MPa (D1) and 20.279 MPa

(D2) of matric potentials, and the control (C).

The ecophysiological parameters were measured once per week over a 5-week period

starting 70 days after sowing (May 20), using the following methods and equipment:

growth parameters (terminology of Hunt, 1990); stomatal resistance (Dynamic Diffusion

Porometer DT AP3); leaf water potential (thermocouple psychrometer WESCOR

HR-33T); and chlorophyll fluorescence (Portable Fluorometer PAM-2000 Heinz Walz

GmbH). The soil water content was controlled through tensiometers, gravimetric method,

and soil psychrometers.

RESULTS

Growth Parameters

Table 1shows that the saline stress-induced plants were less her used than drought-

stressed plants. Although common responses of plants to moderate to relatively high

Bosque Sanchez et al.112



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Table 1. Total biomass yield (TBY, g.plant21), relative growth rate (RGR), leaf area ratio (LAR, cm2.g21), root:shoot ratio (RSR), and fresh

weight:dry weight ratios (FW:DW) on TBY, shoot, and root of Chenopodium quinoa Willd. grown under saline and drought stresses.

TBY (g.pl21)

Treata FW DW RGR LAR (cm2.g21) RSR (g:g) TBY FW:DW Shoot FW:DW Root FW:DW

C 53.27 ^ 11.9 8.50 ^ 1.92 2.20 ^ 0.72 75.73 ^ 6.08 1.73 ^ 0.08 6.27 ^ 0.20 6.62 ^ 0.20 3.75 ^ 0.12

S1 69.64 ^ 3.83 11.26 ^ 0.44 3.23 ^ 0.17 87.06 ^ 26.9 1.79 ^ 0.06 6.18 ^ 0.13 6.54 ^ 0.09 3.66 ^ 0.18

S2 62.66 ^ 3.81 10.14 ^ 0.56 2.81 ^ 0.21 60.31 ^ 12.7 1.70 ^ 0.11 6.18 ^ 0.18 6.50 ^ 0.11 3.73 ^ 0.34

D1 41.04 ^ 3.34 6.87 ^ 0.56 1.58 ^ 0.21 57.55 ^ 6.30 1.81 ^ 0.10 5.98 ^ 0.15 6.39 ^ 0.18 3.53 ^ 0.19

D2 37.41 ^ 6.59 6.31 ^ 1.32 1.37 ^ 0.50 58.49 ^ 6.18 1.82 ^ 0.10 5.96 ^ 0.19 6.29 ^ 0.20 3.40 ^ 0.11

Stat.b ** ** * ** ** ** * *

a C: Control; S1: low salinity; S2: high salinity; D1: low drought stress; D2: high drought stress.b Statistically significant from control at 0.01 (**) and 0.05 (*).

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concentrations of salt are growth reduction and interference in plant nutrition (Shannon,

1992), our results indicated the contrary. Muns and Termaat (1986) showed that the

earliest response of a nonhalophytic plant to salinity is a slow leaf growth. However,

Gorham (1996) found that inhibition of cell expansion and reduction of the leaf area

available for photosynthesis appear to be the most important limitations. Salinity increases

hydraulic conductivity (Evlagon et al., 1990), and probably, the salinity and increased ion

uptake were responsible for the higher overall growth increase of Ch. quinoa. These

findings show that quinoa belongs to the group of halophytic plants.

Drought stress is known to decrease leaf production and size, increase the rate of leaf

death, and reduce plant height and top and root dry weights in several crop species

(Fresnillo Fedorenko et al., 1995). Blum and Sullivan (1997) studied the response of wheat

to drought and found that the stress condition caused a reduction in shoot biomass and

increased total root length. Blum et al. (1997) showed that plant size affected drought

tolerance. In our findings, drought tolerance in quinoa was enhanced by a decrease in

growth rate and plant size.

Stomatal Resistance (rs)

Ch. quinoa has amphistomatous leaves and anomocytic stomata with randomly

orientated pore. As seen in Fig. 1, there is a general tendency in drought- and saline-

stressed plants at level 2 (D2 and S2) to have higher stomatal resistances. Garcia et al.

(1992) found that the rs values in Ch. quinoa are lower under drought conditions than when

irrigated. Espındola (1986) found that the transpiration rate in quinoa reduced and the

water vapor diffusion resistance increased as the soil water deficit increased. Barbe (1998)

noted that transpiration rate in seedlings of quinoa was reduced when the soil water

content was reduced. Lal and Edwards (1996) found that upon withholding water, stomatal

conductance and transpiration declined throughout the drought stress period in Z. mays

and A. cruentus.

In Ch. Quinoa, these comparisons indicate that highly saline- and drought-stressed

plants (S2 and D2) experience a reduction of transpiration rate by increasing rs, which

helps the plants to survive the water deficit. The low rs values found for the S1 treatment

may not signify stress but rather a positive effect at this level of salinity and soil water

content.

Leaf Water Potential (Cl)

Table 2summarizes the water potentials obtained during the five weekly

measurements.

Cl differed only slightly between the treatments, with the general tendency that leaves

with drought stress levels 2 (D2) and 1 (D1), and saline stress level 2 (S2) had slightly

lower Cl. The treatment of saline-stress at level 1 (S1) tended to have the highest Cl,

related to the highest consumption of water during the experimental period. However,

none of the differences were statistically significant ðp . 0:05Þ:




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Figure 1. Stomatal resistances of Ch. quinoa from the first and the last measurements. C: Control;

S1: low salinity; S2: high salinity; D1: low drought stress; D2: high drought stress.

Table 2. Leaf water potentials (Mpa; average ^ standard deviation) during five weekly

measurements in Chenopodium quinoa.

Treata May 22 May 29 June 6 June 11 June 19

C 21.34 ^ 0.14 21.28 ^ 0.12 21.50 ^ 0.06 21.20 ^ 0.16 21.46 ^ 0.07

S1 21.31 ^ 0.17 21.19 ^ 0.19 21.59 ^ 0.20 21.27 ^ 0.12 21.38 ^ 0.10

S2 21.46 ^ 0.12 21.41 ^ 0.14 21.85 ^ 0.02 21.40 ^ 0.13 21.88 ^ 0.12

D1 21.49 ^ 0.10 21.49 ^ 0.03 21.69 ^ 0.19 21.45 ^ 0.05 21.42 ^ 0.25

D2 21.52 ^ 0.12 21.81 ^ 0.15 21.91 ^ 0.32 21.32 ^ 0.26 21.89 ^ 0.30

Statb ns ns ns ns ns

a C: control; S1: low salinity; S2: high salinity; D1: low drought stress; D2: high drought stress.b ns: statistically not significant differences between treatments (,0.05).

Drought and Salinity Stress 115



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Espındola (1986) determined the lowest value of Cl in Ch. quinoa to be 24.2 MPa

when Csoil was 211.1 MPa, which is 4.7% lower than PWP. Garcia et al. (1992) showed

that irrigated quinoa plants have Cl between 21.0 and 22.5 Mpa, whereas in nonirrigated

plants, C1 varied from 21.5–3.2 MPa. In halophytes, besides the decrease in Cl, much of

the excess salt in the leaves is concentrated and crystallized in special bladder cells

(Pasternak and Nerd, 1996). This salt is not active in the metabolism of the leaves, and the

salt that is “compartmentalized” in other tissues or organelles is not active. In Ch. Quinoa,

perhaps the most elaborate adaptation to salinity and drought is the formation of salt-

excreting structures, or the salt glands (bladders) on leaf surfaces, and its important

influence in plant water retention.

Table 3. Variable to maximal fluorescence ratio (Fv/Fm) according to drought and salinity levels;

mean values of five weekly measurements.

May 20 May 27 June 3 June 10 June 17

Treatmentsa Fv/Fm ^ SD Fv/Fm ^ SD Fv/Fm ^ SD Fv/Fm ^ SD Fv/Fm ^ SD

C 0.822 ^ 0.009 0.831 ^ 0.002 0.812 ^ 0.012 0.828 ^ 0.005 0.826 ^ 0.008

S1 0.820 ^ 0.016 0.830 ^ 0.008 0.832 ^ 0.006 0.827 ^ 0.009 0.838 ^ 0.005

S2 0.834 ^ 0.010 0.836 ^ 0.008 0.833 ^ 0.006 0.825 ^ 0.010 0.833 ^ 0.008

D1 0.824 ^ 0.003 0.827 ^ 0.004 0.823 ^ 0.007 0.821 ^ 0.011 0.831 ^ 0.010

D2 0.816 ^ 0.002 0.833 ^ 0.005 0.826 ^ 0.003 0.813 ^ 0.003 0.829 ^ 0.003

Stat.b ns ns ns ns ns

a C: control; S1: low salinity; S2: high salinity; D1: low drought stress; D2: high drought stress.b ns: statistically no significant differences between treatments.

Figure 2. Variable (Fv) to maximum (Fm) fluorescence ratios of Chenopodium quinoa under

drought (——) and salt (– –) stresses. Controls (W); drought stress level 1, D1 (A); drought stress

level 2, D2 (B); salt stress level 1, S1 (S); and salt stress level 2, S2 (V). Measurements on May 27

(second week).




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Chlorophyll Fluorescence Analysis

The advent of “stress meters” has allowed the rapid determination of fluorescence

quenching parameters, especially the ratio of variable to maximal fluorescence, Fv/Fm

(Hovenden and Seppelt, 1995). With the modulated fluorescence technique, the

photochemical (qP) and nonphotochemical (qN) coefficients of fluorescence quenching,

as well as photochemical quantum yield, and the regular Kautsky curve can be determined

(Lichtenthaler, 1992). In the present study, our analysis was focused on the Fv/Fm ratio and

quenching coefficients (qP and qN).

The weekly values of Fv/Fm (Table 3) showed no significant differences between

treatments. However, the salt-treated plants in general, had slightly higher Fv/Fm ratios

than the control (Fig. 2). Droughted plants had a slightly lower Fv/Fm than salt-stressed

plants, suggesting a decrease in the maximum quantum efficiency of open PSII centers as

Figure 3. Photochemical, qP (a, b) and nonphotochemical, qN (c, d) chlorophyll fluorescence

quenching in Chenopodium quinoa Willd. under salt (a, c) and drought (b, d) stresses. Controls (W);

drought stress level 1, D1 (A); drought stress level 2, D2 (B); salt stress level 1, S1 (S); and salt

stress level 2, S2 (V). Data of June 17 (5th week).




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well as an increase in energy dissipation as heat. However, in Ch. quinoa under drought

and salt stresses, the Fv/Fm ratio was not significantly affected. Further studies are

necessary with higher levels of stress and under natural conditions.

Typical changes in the quenching coefficients, qP and qN, are illustrated in Fig. 3. The

only difference was observed for qN quenching in drought-stressed plants, which showed

a steeper decrease than in salt-stressed plants. This indicates that salt-stressed plants have

better protection to photoinhibition at the level of the reaction center of PSII than

droughted plants.

The present study demonstrates that C. quinoa Willd. is a facultative halophyte rather

than a glycophyte. Salt glands/bladders play an important role in plant–water relations. C.

quinoa has good adaptation to drought conditions; however, these strategies result in lower

maximum grain yield. C. quinoa not only offers the possibility of being a useful alternative

crop, but also, through an understanding of its physiology, may provide possible routes to

increasing salt tolerance and drought resistance in other crops.

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drought stress. I. Root drying. Aust. J. Plant Physiol. 24:35–41.

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Ecophysiological Analysis Of Drought And Salinity Stress Of Quinoa ( Chenopodium Quinoa willd.)