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Scientia Agricola

On-line version ISSN 1678-992X

Sci. agric. (Piracicaba, Braz.) vol.78 no.5 Piracicaba  2021  Epub Aug 24, 2020

https://doi.org/10.1590/1678-992x-2019-0338 

Crop Science

Upland rice: phenotypic diversity for drought tolerance

Anna Cristina Lanna1  * 
http://orcid.org/0000-0001-8018-9349

Gesimária Ribeiro Costa Coelho1 
http://orcid.org/0000-0003-3931-3445

Alécio Souza Moreira2 
http://orcid.org/0000-0002-0414-9852

Thiago Gledson Rios Terra3 
http://orcid.org/0000-0003-0428-3100

Claudio Brondani1 
http://orcid.org/0000-0001-6954-6608

Gabriel Rios Saraiva4 
http://orcid.org/0000-0003-3772-1090

Frederico da Silva Lemos4 

Paulo Henrique Ramos Guimarães5 
http://orcid.org/0000-0001-7628-4853

Odilon Peixoto Morais Júnior5 
http://orcid.org/0000-0001-7176-6124

Rosana Pereira Vianello1 
http://orcid.org/0000-0003-0644-5652

1Embrapa Arroz e Feijão, Rod. GO-462, km 12, C.P. 179 – 75375-000 – Santo Antônio de Goiás, GO – Brasil.

2Embrapa Mandioca e Fruticultura, Av. Doutor Ademar Pereira de Barros, 528/529 – 14807-040 – Araraquara, SP – Brasil.

3Universidade Federal do Tocantins – Lab. de Plantas Infestantes, Chácara 69-72, R. Badejos, s/n, Lote 7 – 77404-970 – Gurupi, TO – Brasil.

4Uni-Ahanguera/Centro Universitário de Goiás – Depto. de Ciência Exatas, Biológicas e da Saúde, R. Cândido de Oliveira, 115 – 74423-115 – Goiânia, GO – Brasil.

5Universdiade Federal de Goiás – Depto. de Genética e Melhoramento de Plantas, Rod. GO-462, km 0 – 74001-970 – Goiânia, GO – Brasil.


ABSTRACT:

Upland rice is cultivated mostly in Latin America and Africa by small farmers and in areas with risk of dry spells. This study evaluated morphophysiological mechanisms of upland rice associated to drought adaptation. A set of 25 upland rice genotypes were grown in a plant phenotyping platform during 2015 and 2017 under regular irrigation and water restriction. We evaluated morphophysiological traits in shoots (vegetative structures growth, gas exchange, water use efficiency, carboxylation efficiency, water status) and roots (length, surface area, volume and diameter), as well as agronomic traits (grain yield and its components). There was a reduction in grain yield by up to 54 % and 58 % in 2015 and 2017, respectively, under water deficit. Five upland rice genotypes with the best yield performances in both water treatments applied were recommended to the upland rice-breeding program: Bico Ganga, BRS Esmeralda, BRSMG Curinga, Guarani, and Rabo de Burro. In this study, morphophysiological traits associated to drought tolerance concerned the plant high capacity to save water in the leaves, low leaf water potential, high ability to reduce vegetative structures, high water use efficiency, high photosynthetic capacity, and improved capacity to absorb water from drying soil, either by osmotic adjustment or additional investment into the root system. Therefore, we concluded that different secondary traits contributed to drought tolerance and should be evaluated along with grain yield to improve efficiency of breeding selection.

Keywords: grain yield; gas exchange; water status; root system; vegetative morphology

Introduction

Rice (Oryza sativa L.) is essential for food security for more than half of the world's population (Jumaa et al., 2019). Since rice has an evolutionary peculiarity of semi-aquatic, flooded rice paddies have become the major form of cultivation, growing in irrigated and rainfed lowland conditions, equivalent to 75 % and 19 % of the global production area, respectively (Kikuta et al., 2016). Increasing grain yield of irrigated areas is not enough to supply future demand for rice; furthermore, expansion of production areas is restricted, due to the water scarcity (Parthasarathi et al., 2012). Upland rice represents 4 % of the global rice production and is grown less than 9 % of total rice acreage in Asia, 46 % in Latin America, and 47 % in West Africa (Kikuta et al., 2016). According to Singh et al. (2014), upland rice accounts for 84 % of the total area in Sub-Saharan Africa and it is cultivated mostly by smallholder farms with an average area smaller than 0.5 ha. On the other hand, in Latin America, upland rice is cultivated in large-areas of mechanized harvesting (Bernier et al., 2008).

Drought is one of the most severe abiotic stresses limiting rice yield worldwide and poses a serious threat to rice sustainability in rainfed agriculture (Wu and Cheng, 2014). According to Heinemann et al. (2015), rice yield in upland cultivation (tropical regions mainly) has its yield potential reduced by up to 35 % due to drought-stress conditions.

Reduction in water availability for plants results in a complex response characterized by a decrease in the water potential of its tissues, leading to several changes in different plant processes (Rosales et al., 2012). Some processes reported for upland rice are (a) appropriate phenological patterns that combine crop growth and the amount of water available in the soil (water environment), (b) deep root system, (c) thick stems and reduced number of stomata, (d) osmotic adjustment to maintain cell homeostasis and, consequently, avoid a rapid decrease in leaf-water potential, and (e) senescence delay, also known as stay-green trait, which allows the maintenance of the photosynthetic capacity and the photoassimilate remobilization for a longer time period (Fukai and Cooper, 1995; Boonjung and Fukai, 1996).

Thus, the establishment of sustainable crop systems of upland rice requires better understand of changes in the morphophysiological mechanisms, contributing to drought tolerance and yield effects. This study aimed to (a) identify a series of morphophysiological and agronomic traits related to drought tolerance in upland rice genotypes of Embrapa Core Collection under greenhouse cultivation, and (b) characterize morphophysiological components to be used as indicators for drought tolerance for plant breeding processes.

Materials and Methods

Germplasm

We used 25 accessions of upland rice (Oryza sativa L.) with different responses to drought, obtained through previous field experiments (Bueno et al., 2012). The accessions were represented by 16 landraces, six commercial cultivars from the Embrapa rice-breeding program and three international lines from France and Africa (Table 1). The genotypes were categorized in five phenological groups based on days for the beginning of the reproductive stage (R2 - collar formation on flag leaf/ R3 - panicle exsertion) (Counce et al., 2000).

Table 1 Information on 25 upland rice (Oryza sativa L.) genotypes, categorized into five phenological groups, in both years of trials, 2015 and 2017: genotype identification (ID), code, subspecies, R2/R3 and R8/R9 reproductive stages (DAE, days after emergence), germplasm type, origin, and water deficit period. 

Year Group ID Code Sub specie R2/R3 R8/R9 Germplasm type Origin Drought period
2015 I Arroz Carolino BGA013061 Tropical Japonica 51 91 Landrace Brazil 31/03 - 14/04/2015
Três Meses Branco BGA011901 Tropical Japonica 51 91 Landrace Pitangueiras/SP-Brazil
BRS Soberana BGA008711 Tropical Japonica 51 91 Cultivar Santo Antônio de Goias/GO-Brazil
Aimoré BGA007119 Tropical Japonica 51 91 Landrace Santo Antônio de Goias/GO-Brazil
CIRAD 392 IRGC121727 Tropical Japonica 51 91 Cultivar França
Branquinho 90 Dias BGA011897 Tropical Japonica 51 91 Landrace Batatais/SP-Brazil
Tangará BGA005180 Tropical Japonica 51 91 Landrace Santo Antônio de Goias/GO-Brazil
II IRAT 112 BGA006574 Tropical Japonica 53 94 Cultivar França 02/04 - 16/04/2015
Comum BGA011951 Tropical Japonica 53 94 Landrace Cajazeiras/PB-Brazil
Arroz 4 Meses BGA013769 Tropical Japonica 53 94 Landrace Itaguara/MG-Brazil
Casca Branca BGA013771 Tropical Japonica 53 94 Landrace Piracema/MG-Brazil
Rio Doce BGA004168 Tropical Japonica 53 94 Landrace Santo Antônio de Goias/GO-Brazil
Guarani BGA004121 Tropical Japonica 53 94 Landrace Santo Antônio de Goias/GO-Brazil
Carajás BGA006701 Tropical Japonica 53 94 Landrace Santo Antônio de Goias/GO-Brazil
III BRS Primavera BGA008070 Tropical Japonica 61 101 Cultivar Santo Antônio de Goias/GO-Brazil 09/04 - 23/04/2015
BRS Serra Dourada BGA014150 Tropical Japonica 61 101 Cultivar EMBRAPA-UFG-Brazil
Amarelão BGA011242 Tropical Japonica 61 101 Landrace Bonito/MS-Brazil
Bico Ganga BGA013753 Tropical Japonica 61 101 Landrace Pontalina/GO-Brazil
IV BRSMG Curinga BGA008812 Tropical Japonica 67 107 Cultivar EMBRAPA-EPAMIG/Brazil 16/04 - 30/04/2015
Agulhão BGA013020 Tropical Japonica 67 107 Landrace Caracaraí/RR-Brazil
BRS Esmeralda BGA015465 Tropical Japonica 67 107 Cultivar Santo Antônio de Goias/GO-Brazil
V Douradão BGA012711 Tropical Japonica 80 120 Cultivar Rio Pomba/MG-Brazil 29/04 - 13/05/2015
Saia Velha BGA012954 Tropical Japonica 81 121 Landrace Brejinho/MA-Brazil
Rabo de Burro BGA012426 Tropical Japonica 79 109 Landrace São João dos Patos/MA-Brazil
Moroberekan BGA002524 Tropical Japonica 85 125 Cultivar Africa
2017 I Arroz Carolino BGA013061 Tropical Japonica 44 103 Landrace Brazil 03/10 - 17/10/2017
Três Meses Branco BGA011901 Tropical Japonica 44 103 Landrace Pitangueiras/SP-Brazil
Arroz 4 Meses BGA013769 Tropical Japonica 44 103 Landrace Itaguara/MG-Brazil
Rio Doce BGA004168 Tropical Japonica 44 103 Landrace Santo Antônio de Goias/GO-Brazil
CIRAD 392 IRGC121727 Tropical Japonica 44 103 Cultivar França
Douradão BGA005166 Tropical Japonica 44 103 Cultivar Rio Pomba/MG-Brazil
Tangará BGA005180 Tropical Japonica 44 103 Landrace Santo Antônio de Goias/GO-Brazil
II IRAT 112 BGA006574 Tropical Japonica 47 110 Cultivar França 06/10- 20/10/2017
Aimoré BGA007119 Tropical Japonica 47 110 Landrace Santo Antônio de Goias/GO-Brazil
Casca Branca BGA013771 Tropical Japonica 47 110 Landrace Piracema/MG-Brazil
Branquinho 90 Dias BGA011897 Tropical Japonica 47 110 Landrace Batatais/SP-Brazil
Guarani BGA004121 Tropical Japonica 47 110 Landrace Santo Antônio de Goias/GO-Brazil
III BRS Primavera BGA008070 Tropical Japonica 53 115 Cultivar Santo Antônio de Goias/GO-Brazil 12/10 - 26/10/2017
Comum BGA011951 Tropical Japonica 53 115 Landrace Cajazeiras/PB-Brazil
Carajás BGA006701 Tropical Japonica 53 115 Landrace Santo Antônio de Goias/GO-Brazil
Amarelão BGA011242 Tropical Japonica 53 115 Landrace Bonito/MS-Brazil
Bico Ganga BGA013753 Tropical Japonica 53 115 Landrace Pontalina/GO-Brazil
IV BRSMG Curinga BGA008812 Tropical Japonica 60 126 Cultivar EMBRAPA-EPAMIG/Brazil 19/10 - 02/11/2017
Agulhão BGA013020 Tropical Japonica 60 126 Landrace Caracaraí/RR-Brazil
Rabo de Burro BGA012426 Tropical Japonica 60 126 Landrace São João dos Patos/MA-Brazil
BRS Serra Dourada BGA014150 Tropical Japonica 60 126 Cultivar EMBRAPA-UFG-Brazil
BRS Esmeralda BGA015465 Tropical Japonica 60 126 Cultivar Santo Antônio de Goias/GO-Brazil
V Saia Velha BGA012954 Tropical Japonica 70 133 Landrace Brejinho/MA-Brazil 27/10 - 10/11/2017
BRS Soberana BGA008711 Tropical Japonica 65 128 cultivar Santo Antônio de Goias/GO-Brazil
Moroberekan BGA002524 Tropical Japonica 70 133 Cultivar Africa

Experimental conditions

The experiments were carried out under a greenhouse condition at the plant phenotyping platform facility the Integrated System for Drought-Induced Treatment (Portuguese acronym SITIS) from Feb to June 2015, and from Aug 2017 to Jan 2018, 16°28’00” S, 49°17′00″ W, altitude of 823 m. At the facility, 384 soil columns (diameter: 25 cm; height: 100 cm) were placed on a digital scale to monitor the water amount in each column. The soil, characterized as red latosol (Oxisol), was sieved through 125 mm mesh to remove larger aggregates and it was enriched with minerals, including 1.125 g kg−1 of 5-30-15 formulation, and 0.250 g kg−1 of ammonium sulfate after germination. Urea was applied at the beginning of tillering (V4-V5 stage; 0.350 g kg−1) and in the panicle differentiation (R1 stage; 0.150 g kg−1), four days before the period of water restriction.

The treatments consisted of combinations of two water levels including normal watering (control treatment) and restriction water (stress treatment) conditions. In the control treatment, the amount of soil water was equivalent to 80 % – 85 % of field capacity (FC) established and kept throughout the crop cycle. For the stress treatment, irrigation was performed until the plant reached the reproductive stage (R2/R3), followed by suspension of irrigation for five days, with subsequent replacement of only 50 % of evapotranspirated water at the plate placed on the column bottom for 10 days. The amount of evapotranspirated water was estimated based on the water quantity required to keep soil FC at 80 % – 85 % in the control treatment. Water stress was kept until the control plants reached R6 (grain depth expansion) / R7 (grain dry down) stage. After this period, irrigation was restored until the end of the crop cycle, R8 (at least one grain on the main stem panicle with a brown hull) / R9 (all grains that reached R6 have brown hulls). In the control columns, the evapotranspiration rate was determined daily (difference between the reference mass and the column/day mass) and restored through irrigation placed on the soil surface to achieve the initial mass (reference mass) again. Each column contained three plants.

Agronomic and morphophysiological measurements

Grain yield and yield components

The agronomic traits evaluated were grain yield (GY - g column−1, which means the total mass of grains, in grams, obtained for three plants per column) and its components, such as the number of filled grains (NFG, filled grains average in six panicle column−1), number of empty grains (NEG, empty grains average in six panicle column−1), and 100-grain mass (100GM, g). The last variable was evaluated in 2015. Spikelet sterility was estimated as SS = (NEG × 100) TG−1, where SS = spikelet sterility, NEG = number of empty grains, and TG = total number of grains.

Shoot growth

The following assessments were made for shoot (vegetative structures) growth and reproductive organs traits: (a) leaf area (LA, cm2), average of two flag-leaf of two plants in column, using LI-COR leaf area meter; (b) plant height (PH, cm); (c) tiller number (TN, units); (d) panicle length (PL, cm); (e) shoot dry matter biomass (SDMB, g), through drying samples at 65 °C until a constant weight was achieved and (f) panicle number (PN, units). Data on PH, TN, SDMB, and PN were the average of three plants in the column. Additionally, LA and TN were measured on the last day of water restriction. The PH, PL, SDMB, and PN were obtained at harvesting time. LA and PL were measured in 2015.

Root phenotyping

The root system was evaluated according to the methodology described by Lanna et al. (2016). Briefly, to carry out the root system capture, acrylic tubes were installed inside the columns and three rice plants were planted around the tube. The root system growth was assessed by measuring length (cm), surface area (cm2), volume (cm3) and diameter (mm) of the roots through images generated by CI – 600 root scanner, with quantification by the WinRhizo software. Root images corresponding to depth 1 (5 to 25 cm) and 2 (25 to 45 cm) were taken on the 1st day after irrigation cut-off (phase I), 5th day after irrigation cut-off (phase II) and 10th day after the plants received 50 % of water at the column base (phase III). These parameters were evaluated in 2017.

Gas exchange

Gas exchange rates were taken on flag leaves of two plants in each column and measurements were made using a portable gas exchange analyzer in the infrared region (LCpro+). The parameters measured were: photosynthetic rate (A, μmol CO2 m−2 s−1), transpiration rate (E, mmol H2O m−2 s−1), stomatal conductance (gs, mol H2O m−2 s−1), and internal CO2 concentration (Ci, μmol mol−1). The equipment was set to use temperature and concentrations of 370 - 400 mol mol−1 CO2 in the air, the reference condition used in the IRGA phothosynthesis chamber. The photon flux density photosynthetic active (PPFD) used was 1200 μmol [quanta] m−2 s−1. The minimum equilibration time set for performing the reading was 2 min. Measurements in both control and stressed plants were carried out at from 07h30 to 11h00 a.m. on three evaluation dates during the water deficit period. These dates included the 1st day after irrigation cut-off (phase I), 5th day after irrigation cut-off (phase II), and 10th day after the plants received 50 % of water at the column base (phase III). Water use efficiency (WUE, μmol CO2 mol−1 H2O) was calculated as the ratio between A and gs (Rosales et al., 2012). Carboxylation efficiency (CE, (μmol m−2 s−1) (μmol mol−1)−1) was expressed as the ratio between A and Ci (Silva et al., 2013).

Water status

Leaf water potential (Ψw) was evaluated between 05h00 and 06h00 a.m. using a Scholander pressure chamber (Scholander et al., 1965). The reading was determined at the extremity (tip) of two flag leaves of the primary tiller of two upland rice plants at the end of the water restriction period. Pressure was applied until exudation from the cut made in the leaf collar. Leaf relative water content (RWC, %), osmotic potential (Ψs, MPa), and osmotic adjustment (OA; MPa) were also determined according to the methodology described by Bajji et al., 2001. These parameters were evaluated in 2015.

Experimental design and statistical analysis

All 25 genotypes were evaluated in a 5 × 5 lattice design with 12 repetitions: six repetitions (columns) were for irrigated conditions, and other six repetitions were used for the water deficit treatment, totaling 300 experimental units (with each column containing three plants). Among the six repetitions per water treatment, three repetitions were used for destructive (LA, Ψw, RWC, Ψs and OA; only in 2015) and three for non-destructive measurements (gas exchange, shoot structure, grain yield and its components). For all measurements of shoot traits, transformation √x + 1.0 was applied (where x represents the analyzed variables), which is often used for measurable or count data for normalizing and reducing data skewness (Shapiro and Wilk, 1965, normality test 5 %). The transformed data were subjected to the analysis of variance (ANOVA) based on a fixed linear model and to the joint analysis within each year (2015 and 2017), considering the following: blocks effects, two water levels effects, 25 genotypes, and water level × genotype interaction. The treatment means were compared by the Scott-Knott test (p < 0.05), due to a large number of treatments used in this study, which facilitated the ranking of 25 genotypes into homogeneous groups, without ambiguity. These analyses were carried out using the R platform (R Core Team, 2018). For the root traits, the data were analyzed by the GENES statistical analysis software. The joint analysis of variance was performed between the environments (irrigated and stressed) for each depth, and the significant differences were tested by the Tukey test at p < 0.05.

Results and Discussion

In crops, such as upland rice, where seeds are the product of interest, the main criteria for selecting agronomical tolerance to drought are the traits that lead to higher grain yield. In this study, the analysis of grain yield showed a significant difference (p < 0.05) for all variation sources. For 2015 and 2017, the genotypes accounted for 41 % and 50 % of the total sum of squares, while the environment (water level) accounted for 41 % and 44 % and the genotype versus environment interaction accounted for 18 % and 7 %, respectively. The agronomic performance (grain yield) of genotypes cultivated under two water treatments in 2015 and 2017 is shown in Figures 1A and 1B. In 2015, Bico Ganga, BRS Esmeralda, BRSGO Serra Dourada, BRSMG Curinga, Casca Branca, Guarani, Rabo de Burro, Rio Doce, and Três Meses Branco showed better yield under drought (average grain yield 70.9 g column−1) and irrigated (average grain yield 119.8 g column−1) conditions. In 2017, Agulhão, Bico Ganga, BRS Esmeralda, BRS Primavera, BRS Soberana, BRSMG Curinga, Guarani, and Rabo de Burro were more productive under drought (average grain yield 40.90 g column−1) and irrigated (average grain yield 63.98 g column−1) conditions. Among the upland rice genotypes evaluated, Bico Ganga, BRS Esmeralda, BRSMG Curinga, Guarani, and Rabo de Burro showed better agronomic performance at both water levels in both two years of trials and were then ranked as top genotypes. These genotypes probably present favorable alleles of drought tolerance that may be useful in breeding programs of upland rice. Two of these genotypes are modern cultivars (BRS Esmeralda and BRSMG Curinga), which could be qualified as parents in breeding programs of upland rice. For yield components, the average number of filled-grains and empty-grains was 138 and 46 in 2015, and 266 and 82 in 2017, respectively, in rice cultivated under irrigated condition (Table 2). For plants under drought, the total number of filled-grains and empty-grains were 99 and 37 in 2015, and 184 and 73 in 2017, respectively. The average value of 100-grain weight was 3.03 g under irrigated condition and 2.62 g under stress, determined only in 2015. IRAT 112 (41 %) and Douradão (52 %) presented the highest percentage of spikelet sterility under irrigated condition, and Moroberekan (94 %) and Branquinho 90 Dias (73 %) under drought condition in 2015 and 2017, respectively. In both years of trials, environmental conditions of phenotyping platform SITIS were severe. Particularly in 2017, in addition to artificially imposed water stress, the maximum temperature of 44.7 °C was 6.7 °C higher than the conditions of the 2015 trial, during the water deficit period. In addition, the minimum relative humidity of 26 % was 42 % lower than that of the 2015 trial (Table 3). According to Choudhary et al. (2018), drought commonly occurs combined with other environmental stresses, such as excessive light incidence, heat, and low relative humidity, and characterizes multiplicity of stresses in the tropics. For rice, along with drought, high temperature (up to 33.5 °C) contributed to yield reduction due to the shortening of the vegetative period and high spikelet sterility (Peng et al., 1995; Matsui et al., 1997; Shah et al., 2011).

Figure 1 Grain yield of upland rice (Oryza sativa L.) cultivated in SITIS Platform in years 2015 (A) and 2017 (B). The dotted lines define the average value of grain yield under irrigated and drought conditions. Genotypes that showed higher yield under irrigated and drought conditions were identified in the upper right-hand quadrant in Figures A and B. Bico Ganga, BRS Esmeralda, BRSMG Curinga, Guarani, and Rabo de Burro stood out in both years of trials. 

Table 2 Grain yield (GY; g column−1) and yield components: number of filled grains (NFG; average of six panicles column−1), number of empty grains (NEG; average of six panicles column−1), 100-grain mass (100GM; g), and spikelet sterility (SS; %) of upland rice (Oryza sativa L.) cultivated under irrigated and drought conditions. Trials in 2015 and 2017. 

Genotypes Water level
2015 / 2017
Irrigated Stressed
Yield componentes Yield components
GY NFG NEG 100GM SS GY NFG NEG 100GM SS
Agulhão 153.92Aa / 73.47Aa 158Aa / 257Da 63Aa / 21Db 3.20Aa / - 13.3Bb / 7.7Cb 51.88Ab / 41.48Cb 60Cb / 185Db 25Bb / 64Ca 2.85Aa / - 53.0Ba / 29.3Ca
Aimoré 72.01Da / 46.10Ca 133Ba / 234Da 38Ba / 88Ba 3.14Aa / - 19.7Aa / 27.3Aa 55.27Aa / 27.21Db 123Ba / 100Eb 32Ba / 20Db 2.91Aa / - 24.0Ca / 17.0Ca
Amarelão 123.70Ba / 42.20Ca 128Ba / 238Da 49Aa / 58Ca 3.19Aa / - 16.7Bb / 19.0Ba 50.31Ab / 25.77Db 78Cb / 214Ca 25Ba / 60Ca 3.00Aa / - 38.3Ca / 22.0Ca
Arroz 4 meses 92.77Ca / 51.74Ba 166Aa / 215Da 46Ba / 128Bb 2.89Ba / - 21.7Aa / 37.7Ab 61.44Ab / 27.31Db 115Bb / 87Eb 42Ba / 214Aa 2.72Aa / - 26.7Ca / 71.7Aa
Arroz Carolino 96.11Ca / 49.60Ca 138Ba / 276Da 47Aa / 112Ba 3.13Aa / - 24.0Aa / 29.7Aa 43.10Bb / 21.70Db 108Ba / 259Ca 44Ba / 68Da 2.69Aa / - 29.7Ca / 21.3Ca
Bico Ganga 136.46Ba / 81.57Aa 125Ba / 320Ca 38Ba / 8Da 2.91Ba / - 14.0Ba / 2.7Ca 57.93Ab / 58.78Ab 89Ca / 292Ba 21Ba / 20Ca 2.04Bb / - 30.3 Ca / 6.3Da
Branquinho 90 Dias 96.81Ca / 30.34Da 124Ba / 116Ea 49Aa / 107Bb 3.52Aa / - 30.3Aa / 47.3Ab 67.57Aa / 15.96Db 112Ba / 66Eb 24Ba / 185Aa 2.69Ab / - 16.3Ca / 72.7Aa
BRS Esmeralda 114.47Ca / 64.69Aa 177Aa / 448Ba 55Aa / 68Ca 2.40Ba / - 19.3Ab / 13.3Ba 83.71Ab / 46.45Bb 156Aa / 311Bb 43Ba / 59Ca 2.33Ba / - 26.3Ca / 15.7Da
BRS Primavera 103.04Ca / 71.17Aa 177Aa / 549Aa 67Aa / 71Ca 2.28Ba / - 28.3 Aa/11.0Ba 70.60Ab / 45.33Bb 176Aa / 428Ab 58Ba / 109Ba 2.21Ba / - 24.7Ca / 20.3Ca
BRS Serra Dourada 110.98Ca / 57.29Ba 228Aa / 432Ba 31Ba / 74Bb 2.17Ba / - 11.3Bb / 14.7Bb 69.44Ab / 21.42Db 174Ab / 212Cb 62Bb / 134Ba 2.03Ba / - 27.0Ca / 39.0Ba
BRS Soberana 61.81Da / 67.23Aa 118Ba / 332Ca 61Aa / 49Ca 2.46Ba / - 34.0Aa / 12.7Ba 44.13Ba / 33.61Cb 118Ba / 202Cb 43Ba / 32Da 2.39Ba / - 26.7Ca / 13.7Da
BRSMG Curinga 129.98Ba / 62.71Aa 145Ba / 295Ca 47Ba / 17Da 2.61Aa / - 9.0Ba / 5.3Cb 72.17Ab / 43.37Bb 120Ba / 219Cb 14Bb / 35Da 2.15Ba / - 31.3Ca / 13.3Da
Carajás 103.16Ca / 46.37Ca 165Aa / 236Da 48Ba / 90Ba 3.19Aa / - 11.3Bb / 27.7Ab 55.43Ab / 17.19Db 93Cb / 107Eb 22Ba / 114Ba 2.79Aa / - 37.0Ca / 52.0Ba
Casca Branca 113.45Ca / 55.23Ba 157Aa / 244Da 51Aa / 118Ba 3.52Aa / - 21.3Aa / 34.0Aa 66.65Ab / 21.45Db 135Ba / 159Db 42Ba / 51Cb 2.96Aa / - 28.0Ca / 23.7Ca
Cirad 392 87.02Ca / 48.56Ca 124Ba / 222Da 46Ba / 101Ba 2.87Ba / - 12.7Bb / 31.0Aa 53.07Ab / 23.54Db 106Ba / 136Db 17Bb / 70Ca 2.83Aa / - 30.7Ca / 34.0Ba
Comum 9.53Da / 41.72Ca 56Ca / 255Da 13Ba / 36Da 3.45Aa / - 6.3Ba / 11.7Ba 6.85Ca / 22.31Db -/ 176Db -/ 43Da -/- - / 19.7Ca
Douradão 108.77Ca / 1.86Ca 120Ba / 132Ea 46Ba / 156Aa 2.76Ba / - 11.0Bb / 52.3Aa 34.68Bb / 20.14Db 50Cb / 102Ea 15Bb / 129Ba 2.07Bb / - 48.0Ba / 52.7Ba
Guarani 105.75Ca / 37.18Da 109Ba / 146Ea 43Ba / 84Ba 3.74Aa / - 14.0Bb / 36.7Aa 59.65Ab / 22.88Db 81Ca / 138Da 18Ba / 64Ca 3.23Aa / - 34.7Ca / 32.0Ca
IRAT 112 72.37Da / 46.70Ca 91Ba / 185Ea 56Aa / 125Ba 3.80Aa / - 41.0Aa / 40.3Aa 66.80Aa / 19.12Db 82Ca / 143Da 35Ba / 45Cb 3.37Aa / - 27.7Ca / 26.3Cb
Moroberekan 44.18Da / 33.79Da 111Ba / 263Da 47Aa / 26Da 2.89Ba / - 30.0Ab / 9.3Cb 4.08Cb / 27.32Da 7Db / 169Db 117Ab / 54Ca 2.14Bb / - 94.0Aa / 24.0Ca
Rabo de Burro 152.69Aa / 53.78Ba 173Aa / 367Ca 58Ba / 66Ca 3.21Aa / - 8.3Bb / 14.7Ba 83.79Ab / 35.35Cb 104Bb / 373Aa 16Bb / 60Ca 2.86Aa / - 38.0Ca / 13.7Da
Rio Doce 105.75Ca / 52.29Ba 139Ba / 297Ca 49Aa / 214Aa 3.33Aa / - 25.0Aa / 42.0Aa 59.25Ab / 36.94Cb 125Ba / 214Cb 46Ba / 46Cb 2.61Ab / - 28.0Ca / 17.3Db
Saia Velha 170.02Aa / 25.30Da 119Ba / 155Ea 26Ba / 63Ca 2.35Ba / - 17.7Aa / 28.7Aa 26.93Bb / 25.30Da 19Db / 105Ea 92Ab / 60Ca 2.34 Ba / - 83.0Ab / 35.7Ba
Tangará 91.70Ca / 49.08Ca 123Ba / 219Da 33Ba / 59Ca 3.77Aa / - 21.7Aa / 21.0Ba 60.96Ab / 30.98Db 104Ba / 122Db 30Ba / 35Da 2.73Ab / - 23.0Ca / 22.3Ca
Três Meses Branco 108.79Ca / 37.60Da 145Ba / 205Da 40Ba / 100Ba 3.48Aa / - 22.0Aa / 32.7Aa 86.67Aa / 20.79Db 144Aa / 86Eb 32Ba / 60Ca 3.0Aa / - 18.3Ca / 42.7Ba

Capital letters compare the genotypes within each water regime and small letters the water levels within each genotype. Means followed by the same capital letter in the column and means followed by the same letter on the lines not differ by the Scott-Knott test 5% error probability. Transformed data in square root of Y+1.0SQRT (Y+1.0) to statistical analysis.

Table 3 Climatic variables on the phenotyping platform SITIS on growth of upland rice (Oryza sativa L.), including temperature and relative humidity, maximum and minimum values. Upland rice (A and C) and drought period (B and D), in 2015 and 2017. 

Climatic condition T max T min RH max RH min
---------------- °C ----------------- ----------------- % -----------------
2015
Upland rice cycleA 37.5 21.5 81.3 40.9
Drought periodB 38.0 22.4 84.3 44.6
2017
Upland rice cycleC 43.4 22.1 66.9 27.6
Drought periodD 44.7 23.3 62.7 26.0

A02 Feb to 15 June, 2015

B31 Mar to 13 May, 2015

C21 Aug, 2017 to 19 Jan, 2018

D03 Oct to 10 Nov, 2017.

According to Bernier et al. (2008), practices based on the assessment of agronomic performance of crop species require a long procedure, which limits breeding efficiency. Thus, a better understand of mechanisms of drought tolerance is necessary, since the association between main (grain yield and its components) and secondary (morphophysiology) traits could provide greater selection efficiency. For this, identifying morphophysiological traits related to drought tolerance is relevant to assist in the identification of mechanisms underlying these adaptation processes and thus in the selection of tolerant genotypes. In this study, upland rice plants reacted to drought stress by slowing down their growth (Table 4). In 2015, most genotypes (Agulhão, Aimoré, Amarelão, Arroz 4 meses, Bico Ganga, BRS Esmeralda, Primavera, BRSMG Curinga, Carajás, Casca Branca, Cirad 392, Douradão, Guarani, Moroberekan, Rabo de Burro, Rio Doce, Tangará, and Três Meses Branco) showed reduced PH (14 % on average) under drought condition. While, in 2017, only six genotypes (Agulhão, Bico Ganga, BRS Serra Dourada, Carajás, Rabo de Burro, and Rio Doce) presented an average reduction of 12 %. Overall, there was no difference between plants grown under both water levels for SDMB, TN, and PN, in both years of trials. Parameters LA and PL, taken in 2015, showed reductions of 13 % and 3 %. LA and PH were the main morphological traits affected by drought stress in top genotypes Bico Ganga, BRS Esmeralda, BRSMG Curinga, Guarani, and Rabo de Burro, in both years of trials. According to Fischer et al. (2003) and Chaves et al. (2009), reduction of leaf growth and stem elongation in rice plants are the first processes affected by drought and could be considered as a tolerance mechanism, since they reduce the transpiration capacity, and consequently, plant demand for water. Furthermore, slowed growth (due to reduction of stomatal conductance, CO2 assimilation and, consequently, photoassimilates production and accumulation) has been suggested as an adaptive trait for plant survival under stress. This trait allows plants to divert assimilates and energy into protective molecules to deal with stress (Zhu, 2002) and/or keep root growth by increasing water acquisition (Chaves et al., 2003; Pandey and Shukla, 2015).

Table 4 Shoot dry matter biomass (SDBM, g), leaf area (LA, cm2), plant height (PH, cm), tiller number (TN, unit), panicle number (PN, unit), and panicle length (PL, cm) of upland rice (Orysa sativa L.) grown under irrigated and drought conditions. Trials in 2015 and 2017. 

Genotypes Water level
2015 / 2017
Irrigated Stressed
SDBM LA PH TN PN PL SDBM LA PH TN PN PL
Agulhão 140.24 Ba/112.24 Ba 85.7127 Aa/ - 136.9 Ba/129.3 Aa 14.1 Aa/13.2 Aa 12.3 Aa/11.3 Aa 29.6 Aa/ - 135.33 Ba/112.60 Ba 70.8553 Aa/ - 109.8 Bb/108.2 Bb 14.3 Ba/14.8 Ca 13.1 Ba/11.0 Aa 24.8 Bb/ -
Aimoré 59.33 Ca/41.48 Da 54.3373 Ca/ - 120.9 Ca/80.5 Ea 8.4 Ba/7.8 Cb 8.3 Ba/7.7 Ba 25.0 Ba/ - 54.72 Ca/31.07 Da 51.7803 Aa/ - 104.1 Bb/81.7 Da 8.6 Ca/9.7 Ca 8.1 Da/8.7 Ba 26.4 Aa/ -
Amarelão 127.69 Ca/54.94 Da 86.5447 Aa/ - 145.8 Aa/127.1 Aa 10.7 Ba/7.3 Ca 9.7 Ba/7.3 Ba 27.7 Aa/ - 115.44 Ba/52.36 Ca 48.3237 Bb/ - 132.7 Ab/117.7 Aa 9.3 Ca/5.5 Eb 9.3 Ca/5.3 Db 25.3 Ba/ -
Arroz 4 meses 79.02 Ca/62.50 Ca 87.4770 Aa/ - 153.3 Aa/112.4 Ba 6.8 Ba/7.7 Ca 6.7 Ba/7.3 Ba 30.6 Aa/ - 70.36 Ca/49.01 Ca 76.4233 Aa/ - 123.9 Ab/103.4 Ba 7.6 Ca/7.6 Da 7.55 Da/7.0 Ca 26.4 Ab/ -
Arroz Carolino 72.59 Ca/55.03 Da 66.6093 Ba/ - 140.0 Ba/105.7 Ca 9.2 Ba/7.5 Cb 9.2 Ba/6.3 Ba 29.4 Aa/ - 71.64 Ca/49.97 Ca 60.5197 Aa/ - 129.6 Aa/98.2 Ca 9.5 Ca/9.7 Ca 9.1 Ca/6.3 Ca 30.3 Aa/ -
Bico Ganga 138.56 Ba/154.84 Ba 81.5693 Aa/ - 156.9 Aa/139.1 Aa 13.1 Aa/12.9 Aa 13.1 Aa/12.3 Aa 26.3 Ba/ - 135.03 Ba/117.87 Ba 60.2790 Ab/ - 133.4 Ab/121.8 Ab 14.4 Ba/11.5 Ba 15.6 Aa/10.3 Aa 26.1 Ba/ -
Branquinho 90 Dias 74.85 Ca/56.14 Da 54.5883 Ca/ - 136.7 Ba/90.6 Da 9.6 Ba/7.0 Cb 9.6 Ba/7.0 Ba 25.8 Ba/ - 64.71 Ca/38.97 Da 53.9200 Aa/ - 122.3 Aa/82.3 Da 9.0 Ca/8.8 Da 8.9 Ca/8.3 Ba 23.7 Ba/ -
BRS Esmeralda 85.50 Ca/65.00 Ca 54.1700 Ca/ - 121.7 Ca/101.6 Ca 9.9 Ba/9.1 Ca 9.7 Ba/8.7 Ba 29.4 Aa/ - 80.91 Ca/63.25 Ca 38.8567 Ba/ - 106.6 Bb/95.4 Ca 9.9 Ca/9.3 Ca 9.4 Ca/8.7 Ba 25.9 Ab/ -
BRS Primavera 97.86 Ca/72.87 Ca 82.6263 Aa/ - 135.9 Ba/120.0 Ba 9.6 Ba/7.4 Ca 9.2 Ba/7.3 Ba 29.3 Aa/ - 92.33 Ca/58.78 Ca 63.8400 Ab/ - 121.1 Ab/111.2 Ba 10.1 Ca/7.3 Da 9.8 Ca/5.7 Da 28.1 Aa/ -
BRS Serra Dourada 93.29 Ca/61.87 Ca 71.7250 Ba/ - 113.7 Ca/104.9 Ca 9.8 Ba/8.6 Ca 9.8 Ba/8.3 Ba 29.5 Aa/ - 89.99 Ca/47.81 Ca 61.6593 Aa/ - 111.0 Ba/91.4 Cb 9.2 Ca/9.6 Ca 9.8 Ca/8.0 Ba 27.8 Aa/ -
BRS Soberana 64.71 Ca/73.11 Ca 55.8537 Ca/ - 138.8 Ba/86.8 Da 8.1 Ba/12.6 Aa 8.1 Ba/12.0 Aa 27.5 Aa/ - 63.63 Ca/59.34 Ca 50.1880 Aa/ - 130.1 Aa/79.7 Da 7.9 Ca/11.4 Ba 7.7 Da/9.3 Bb 28.3 Aa/ -
BRSMG Curinga 120.3 Ba/78.91 Ca 76.4703 Ba/ - 114.2 Da/98.7 Ca 15.5 Aa/13.1 Aa 12.6 Aa/12.7 Aa 25.7 Ba/ - 119.13 Ba/70.13 Ca 49.2980 Bb/ - 95.0 Cb/89.7 Ca 17.7 Aa/11.6 Ba 16.4 Ab/11.3 Aa 24.5 Ba/ -
Carajás 77.11 Ca/45.39 Da 71.8847 Ba/ - 138.0 Ba/89.9 Da 9.1 Ba/8.3 Ca 9.0 Ba/8.0 Ba 27.8 Aa/ - 74.67 Ca/42.32 Da 70.6663 Aa/ - 120.2 Ab/79.8 Db 8.0 Ca/10.1 Ca 7.8 Da/8.7 Ba 22.9 Bb/ -
Casca Branca 86.07 Ca/50.48 Da 74.6667 Ba/ - 143.6 Aa/99.8 Ca 8.6 Ba/7.1 Ca 8.3 Ba/7.0 Ba 27.7 Aa/ - 69.55 Ca/44.07 Da 64.3147 Aa/ - 123.0 Ab/92.3 Ca 7.6 Ca/6.8 Ea 7.2 Da/6.7 Ca 25.1 Ba/ -
Cirad 392 76.86 Ca/38.84 Da 55.0230 Ca/ - 127.3 Ca/93.3 Da 14.8 Aa/10.5 Bb 14.4 Aa/10.0 Aa 26.8 Ba/ - 62.83 Ca/34.09 Da 48.3480 Ba/ - 114.9 Bb/91.5 Ca 11.3 Cb/12.6 Ba 10.6 Cb/11.3 Aa 26.2 Aa/ -
Comum 36.88 Da/124.57 Ba 150.0533 Aa/ - 98.0 Da/118.4 Ba 4.7 Ca/7.8 Ca 1.7 Da/7.3 Ba 9.5 Ca/ - 34.51 Da/101.30 Ba 96.2612 Ab/ - 64.43 Ca/119.6 Aa 9.0 Ca/7.3 Da 1.0 Ea/7.0 Ca 9.6 Ca/ -
Douradão 206.06Aa/49.13 Da 54.5177 Ca/ - 145.7 Aa/92.2 Da 13.8 Aa/7.6 Ca 10.2 Ba/7.3 Ba 24.1 Ba/ - 198.27 Aa/39.26 Da 48.6343 Ba/ - 121.0 Ab/86.6 Ca 14.4 Ba/8.4 Da 12.3 Ba/8.3 Ba 20.3 Bb/ -
Guarani 78.22 Ca/53.08 Da 68.3230 Ba/ - 132.8 Ba/91.1 Da 10.0 Ba/7.7 Cb 10.0 Ba/7.7 Ba 28.4 Aa/ - 68.41 Ca/42.99 Da 57.8473 Aa/ - 110.6 Bb/90.0 Ca 9.0 Ca/9.8 Ca 9.0 Ca/9.3 Ba 25.1 Ba/ -
IRAT 112 54.42 Ca/42.13 Da 66.3190 Ba/ - 113.3 Da/81.9 Ea 8.4 Ba/8.2 Ca 8.2 Ba/8.7 Ba 26.0 Ba/ - 52.19 Ca/34.49 Da 64.4373 Aa/ - 112.1 Ba/76.7 Da 7.2 Ca/9.2 Ca 7.2 Da/8.7 Ba 24.5 Ba/ -
Moroberekan 223.75Aa/122.30 Ba 86.1173 Aa/ - 135.6 Ba/119.1 Ba 7.9 Ba/5.8 Ca 6.8 Ba/5.7 Ba 27.6 Aa/ - 169.66 Ab/109.47 Ba 70.3757 Aa/ - 108.2 Bb/115.7 Aa 7.1 Ca/5.9 Ea 3.9 Ea/4.3 Da 26.0 Aa/ -
Rabo de Burro 131.65 Ba/137.37 Ba 58.7113 Ca/ - 149.7 Aa/131.6 Aa 11.3 Ba/7.5 Ca 10.8 Aa/7.0 Ba 28.8 Aa/ - 130.65 Ba/89.34 Ba 38.0407 Bb/ - 126.2 Ab/118.0 Ab 12.6 Ba/5.9 Eb 9.8 Ca/5.3 Da 26.5 Aa/ -
Rio Doce 78.82 Ca/46.67 Da 7.3593 Da/ - 146.3 Aa/106.7 Ca 9.2 Ba/7.8 Ca 9.1 Ba/8.0 Ba 29.0 Aa/ - 70.86 Ca/47.54 Ca 60.2577 Aa/ - 130.0 Ab/95.7 Cb 8.1 Ca/8.4 Da 7.9 Da/8.3 Ba 26.4 Aa/ -
Saia Velha 212.43Aa/300.01 Aa 36.9460 Ca/ - 115.2 Da/135.2 Aa 14.6 Aa/13.2 Aa 11.1 Aa/12.3 Aa 24.1 Ba/ - 209.54 Aa/205.27 Ab 27.1570 Ca/ - 109.1 Ba/123.4 Aa 17.2 Aa/12.2 Ba 15.6 Ab/11.0 Aa 22.9 Ba/ -
Tangará 70.73 Ca/45.98 Da 56.2763 Ca/ - 108.4 Da/75.9 Ea 11.0 Ba/8.1 Ca 10.9 Aa/8.0 Ba 26.6 Ba/ - 69.28 Ca/34.66 Da 55.2497 Aa/ - 98.8 Cb/70.1 Da 10.6 Ca/9.7 Ca 10.3 Ca/9.0 Ba 23.6 Ba/ -
Três Meses Branco 76.83 Ca/40.43 Da 60.4217 Da/ - 130.9 Ba/95.9 Ca 9.2 Ba/6.7 Cb 9.2 Ba/6.7 Ba 28.0 Aa/ - 71.68 Ca/40.05 Da 59.9543 Aa/ - 118.9 Ab/80.8 Ca 9.2 Ca/8.4 Da 8.9 Ca/7.0 Ca 27.5 Aa/ -

Capital letters compare genotypes within each water regime and small letters compare water levels within each genotype. Means followed by the same capital letter in the column and means followed by the same letter on the rows do not differ by the Scott-Knott test 5 % error probability. Transformed data in square root of Y+1.0SQRT (Y+1.0) for the statistical analysis.

The effect of the drought treatment was also evaluated by characterization of the root system, an important organ to increase rice yield under water stress (Pandey and Shukla, 2015; Kundur et al., 2015). According to Kato et al. (2006), rice root is complex, combining various root morphologies and showing considerable genotypic variation, also subjected to environmental effects. Thereby, a deep root system could improve adaptation of upland rice during drought by increasing capacity of extraction water, keeping high leaf water status with better crop performance under drought conditions (Kamoshita et al., 2004; Mishra and Salokhe, 2011). In this study, the analysis of the root system of upland rice showed a significant difference (p < 0.05) for most variation sources. At depth 1 (5 - 25 cm), the genotypes accounted for 14 % of the total sum of squares, the environment (water level) accounted for 54 %, and the double interaction, genotype versus water lever, accounted for 32 %. At depth 2 (25 - 45 cm), the genotypes accounted for 62 % of the total sum of the square, the environment (water level) accounted for 20 %, and the double interaction, genotype versus water level, accounted for 17 %.

The root system properties (length, surface area, volume, and diameter) of upland rice plants during the drought period are shown in Figure 2. Under irrigated condition, the genotypes that stood out mostly in terms of length, area, volume, and root diameter were IRAT 112, Agulhão, BRSMG Curinga (top genotype), Comum, Rabo de Burro (top genotype), and Saia Velha, at both depths. Under drought condition, the highlight was BRSMG Curinga followed by Agulhão, Comum, Rabo de Burro, and Saia Velha. Therefore, among top genotypes, BRSMG Curinga, and Rabo de Burro presented greater robustness of the root system, mainly at depth 2 (25 - 45 cm), irrespective of the water level applied. This is in accordance with Pandey and Shukla (2015), which describe that under water deficit, root growth is usually kept, while shoot growth is inhibited. Conversely, Ji et al. (2012) found a more extensive deeper root growth in a tolerant rice cultivar, IRAT109, after 20 days of irrigation cut-off. The findings of our study indicate a mechanism at the molecular level underlying a constitutive root growth for the root traits evaluated. Water deficit is an important environmental constraint and influences all physiological processes in plant growth, affecting gas exchange mechanisms (Ma et al., 2018).

Figure 2 Root length (cm), Root area (cm2), Root volume (cm3), and Root diameter (mm), at first (soil layer of 5 - 25 cm) and second (soil layer of 25 - 45 cm) depths of the soil cultivated with upland rice (Oryza sativa L.). Plants were grown under irrigated and drought conditions. Capital letters compare genotypes within each water regime and small letters compare water regimes within each genotype. Means followed by the same letter do not differ by the Tukey test 5 % error probability. Parameters were evaluated in 2017. 

The stress effects on A, E, gs, Ci, WUE, and CE in upland rice plants are shown in Table 5. During phase I, where control and stress columns were in similar conditions of soil water availability, there was genetic variability among rice accessions, implying a contrast for the gas exchange traits evaluated, in both years of trials. In 2015, A ranged from 8.34 to 25.31 µmol CO2 m−2 s−1, E ranged from 2.60 to 9.34 mmol H2O m−2 s−1, and gs (number and activity of stomata) ranged from 0.16 to 0.52 mol H2O m−2 s−1. In 2017, 7.95 to 25.91 µmol CO2 m−2 s−1, 4.16 to 11.65 mmol H2O m−2 s−1, and 0.13 to 0.47 mol H2O m−2 s−1, respectively. In phase II, 5th day after irrigation cut-off, we observed mechanisms, such as leaf-rolling and stomatal closure. These events soften the solar radiation incidence and transpiration rate, respectively, increasing water conservation and delaying water deficit. Low values of A, E and gs were observed in both years of trials. In 2015, A ranged from 1.27 to 15.67 µmol CO2 m−2 s−1, E ranged from 0.97 to 4.14 mmol H2O m−2 s−1, and gs ranged from 0.04 to 0.47 mol H2O m−2 s−1. In 2017, A ranged from 0.82 to 19.21 µmol CO2 m−2 s−1, E ranged from 1.07 to 6.27 mmol H2O m−2 s−1, and gs ranged from 0.02 to 0.14 mol H2O m−2 s−1. Four out of five top genotypes (Bico Ganga, BRS Esmeralda, BRSMG Curinga, and Rabo de Burro) showed average reduction of 84 %, 72 %, and 81 % in A, E, and gs, respectively, in plants cultivated under drought. In phase III, after plants under stress received 50 % of water at the column base for 10 days, only three genotypes, Três Meses Branco (2015), Branquinho 90 Dias, and Rabo de Burro (2017) restored the functioning of the photosynthetic machinery, since stressed plants showed values of photosynthetic rate similar to those of irrigated plants. Conversely, for the other genotypes including Bico Ganga, BRS Esmeralda, BRSMG Curinga, and Guarani (top genotypes), recovery of A, E, and gs was 40 %, 46 %, and 30 %, respectively, in stressed plants.

Table 5 Photosynthetic rate (A, μmol CO2 m−2 s−1), transpiratory rate (E, mmol H2O m−2 s−1), stomatal conductance (gs, mol H2O m−2 s−1), internal CO2 concentration (Ci, μmol mol−1), water use efficiency (WUE, μmol CO2 mol−1 H2O), and carboxylation efficiency (CE; (μmol m−2 s−1) (μmol mol−1) −1) of upland rice (Oryza sativa L.). The evaluation during three periods: Phase I - the first day after irrigation cut-off, Phase II - the fifth day after irrigation cut-off, and Phase III - the tenth day after plants received 50 % of water at the column base. Trials in 2015 and 2017. 

Genotypes Phase I
2015 / 2017
Irrigated
A E gs WUE CE
Agulhão 16.35 B / 9.73 C 5.18 D / 4.80 C 0.34 C / 0.17 D 48.1 A / 57.2 B 0.067 A / 0.72 B
Aimoré 21.09 A / 19.71 A 7.97 B / 9.54 B 0.42 B / 0.21 C 50.2 A / 93.3 A 0.080 A / 0.113 A
Amarelão 22.12 A / 18.37 B 5.00 D / 9.34 B 0.60 A / 0.23 C 36.9 A / 79.9 A 0.067 A / 0.090 A
Arroz 4 meses 23.62 A / 21.74 A 6.64 D / 4.71 C 0.47 B / 0.43 A 50.3 A / 50.6 B 0.081 A / 0.087 B
Arroz Carolino 21.19 A / 22.73 A 7.36 C / 6.48 C 0.35 C / 0.42 A 60.5 A / 54.1 B 0.089 A / 0.095 A
Bico Ganga 21.44 A / 11.87 B 5.92 D / 6.79 B 0.52 A / 0.21 D 41.2 A / 56.5 B 0.068 A / 0.069 B
Branquinho 90 Dias 20.74 A / 16.05 B 6.69 D / 5.36 C 0.39 B / 0.26 C 53.2 A / 61.7 B 0.078 A / 0.089 A
BRS Esmeralda 19.21 A / 16.20 B 6.51 D / 7.18 B 0.42 B / 0.20 C 45.7 A / 81.0 A 0.079 A / 0.082 B
BRS Primavera 20.89 A / 12.37 B 6.39 D / 5.86 C 0.50 A / 0.22 D 41.8 A / 56.2 B 0.070 A / 0.069 B
BRS Serra Dourada 25.25 A / 18.90 B 6.43 D / 7.54 B 0.52 A / 0.28 C 48.6 A / 67.5 B 0.089 A / 0.099 A
BRS Soberana 25.31 A / 20.29 A 9.17 A / 11.65 A 0.45 B / 0.26 C 56.2 A / 78.0 B 0.107 A / 0.101 A
BRSMG Curinga 15.26 B / 12.70 B 6.15 D / 4.87 C 0.36 C / 0.14 D 42.4 A / 90.7 A 0.059 B / 0.064 B
Carajás 20.46 A / 16.66 B 6.81 D / 8.44 B 0.42 B / 0.20 C 48.7 A / 83.3 A 0.072 A / 0.087 B
Casca Branca 21.98 A / 16.64 B 6.92 C / 8.17 B 0.40 B / 0.20 C 55.0 A / 93.2 A 0.083 A / 0.104 A
Cirad 392 24.62 A / 25.91 A 9.34 A / 7.65 B 0.45 B / 0.45 A 54.7 A / 57.6 B 0.101 A / 0.108 A
Comum 17.13 B / 16.99 B 6.11 B / 6.99 B 0.39 B / 0.22 C 43.9 A / 77.2 B 0.058 B / 0.078 B
Douradão 13.61 B / 20.26 A 3.61 E / 5.38 C 0.27 D / 0.32 B 50.4 A / 63.3 B 0.048 B / 0.087 A
Guarani 23.12 A / 20.87 A 7.86 B / 8.33 C 0.40 B / 0.23 C 57.8 A / 90.7 A 0.088 A / 0.117 A
IRAT 112 22.46 A / 19.09 B 7.55 C / 6.50 C 0.52 A / 0.26 C 43.2 A / 73.4 B 0.074 A / 0.087 B
Moroberekan 15.82 B / 10.41 C 5.64 D / 6.11 C 0.28 D / 0.13 D 56.5 A / 80.1 A 0.060 B / 0.050 C
Rabo de Burro 16.36 B / 7.95 C 3.93 E / 4.16 C 0.26 D / 0.08 D 62.9 A / 99.4 A 0.067 A / 0.047 C
Rio Doce 19.99 A / 21.85 A 6.98 C / 6.31 C 0.33 C / 0.43 A 60.6 A / 50.8 B 0.079 A / 0.087 B
Saia Velha 8.34 C / 11.60 B 2.60 E / 6.45 C 0.16 D / 0.13 D 52.1 A / 89.2 A 0.028 B / 0.057 C
Tangará 19.69 A / 22.92 A 7.47 C / 6.21 C 0.37 C / 0.47 A 53.2 A / 48.8 B 0.080 A / 0.093 A
Três Meses Branco 22.47 A / 21.07 A 7.46 C / 6.10 C 0.41 B / 0.38 B 54.8 A / 55.4 B 0.088 A / 0.088 B
Genotypes Phase II
2015 / 2017
Irrigated Stressed
A E gs WUE CE A E gs WUE CE
Agulhão 18.88 Aa / 16.06 Ba 4.62 Ca / 4.80 Ba 0.50 Aa / 0.21 Ca 37.8 Aa / 76.5 Ba 0.070 Ba / 0.068 Ba 4.02 Bb / 2.95 Db 1.80 Bb / 1.38 Bb 0.10 Bb / 0.05 Cb 40.2 Aa / 59.0 Ca 0.013 Bb / 0.010 Cb
Aimoré 24.96 Aa / 20.83 Aa 6.78 Ba / 9.72 Aa 0.56 Aa / 0.22 Ca 44.6 Aa / 94.7 A a 0.098 Aa / 0.125 Aa 14.46 Ab / 8.13 Cb 3.91 Ab / 4.56 Ab 0.25 Ab / 0.08 Cb 57.8 Aa / 101.6 Aa 0.055 Ab / 0.037 Bb
Amarelão 19.24 Aa / 17.27 Ba 6.40 Ba / 8.00 Aa 0.43 Aa / 0.17 Ca 44.7 Aa / 101.6 Aa 0.074 Aa / 0.096 Aa 2.21 Bb / 5.40 Cb 1.56 Bb / 3.14 Ab 0. 06 Bb / 0.05 Cb 36.8 Aa / 108.0 Aa 0.004 Bb / 0.026 Cb
Arroz 4 meses 21.17 Aa / 18.19 Aa 4.60 Ca / 8.74 Aa 0.51 Aa / 0.17 Ca 41.5 Aa / 107.0 Aa 0.080 Aa / 0.118 Aa 5.40 Bb / 5.54 Cb 1.35 Bb / 3.61 Ab 0.11 Bb / 0.06 Cb 49.1 Aa / 92.3 Ba 0.019 Bb / 0.044 Bb
Arroz Carolino 25.68 Aa / 22.25 Aa 7.75 Aa / 6.53 Ba 0.46 Aa / 0.28 Ba 55.8 Aa / 79.5 Aa 0.111 Aa / 0.103 Aa 1.27 Bb / 19.21 Aa 1.77 Bb / 6.27 Aa 0.05 Bb / 0.23 Aa 25.4 Aa / 83.5 Ba 0.004 Bb / 0.094 Aa
Bico Ganga 18.64 Ba / 10.13 Ba 7.39 Ba / 4.94 Ba 0.39 Aa / 0.17 Da 47.8 Aa / 59.6 Aa 0.073 Ba / 0.064 Ba 1.32 Bb / 0.62 Db 1.73 Bb / 1.65 Bb 0.05 Bb / 0.02 Ca 26.4 Aa / 31.0 Db 0.004 Bb / 0.002 Cb
Branquinho 90 Dias 21.64 Aa / 16.19 Ba 5.62 Ca / 6.98 Ba 0.49 Aa / 0.16 Ca 44.2 Aa / 101.2 Aa 0.079 Aa / 0.094 Aa 6.89 Bb / 6.56 Cb 1.99 Bb / 2.91 Bb 0.10 Bb / 0.05 Cb 68.9 Aa / 131.2 Aa 0.024 Bb / 0.036 Cb
BRS Esmeralda 20.54 Aa / 14.58 Ba 5.50 Ca / 5.09 Ba 0.58 Aa / 0.16 Ca 35.4 Aa / 91.1 Aa 0.076 Ba / 0.065 Ba 4.45 Bb / 3.28 Db 1.73 Bb / 1.07 Bb 0.09 Bb / 0.02 Cb 49.4 Aa / 164.0 Aa 0.015 Bb / 0.011 Cb
BRS Primavera 20.89 Aa / 12.72 Ba 8.14 Aa / 7.96 Aa 0.39 Aa / 0.13 Da 53.6 Aa / 97.9 Aa 0.091 Aa / 0.069 Ba 1.60 Bb / 0.82 Db 1.48 Bb / 2.03 Bb 0.04 Bb / 0.07 Cb 40.0 Aa / 11.7 Db 0.005 Ab / 0.003 Cb
BRS Serra Dourada 23.23 Aa / 18.34 Aa 8.04 Aa / 6.51 Ba 0.41 Aa / 0.31 Ba 56.7 Aa / 59.2 Ba 0.112 Aa / 0.077 Ba 12.04 Ab / 6.18 Cb 4.14 Ab / 2.18 Bb 0.16 Bb / 0.07 Cb 75.3 Aa / 8 8.3 Ba 0.054 Ab / 0.026 Cb
BRS Soberana 24.76 Aa / 23.51 Aa 9.28 Aa / 9.55 Aa 0.45 Aa / 0.38 Aa 55.0 Aa / 61.9 Ba 0.121 Aa / 0.097 Aa 9.86 Ab / 9.50 Cb 3.75 Ab / 3.78 Ab 0.12 Bb / 0.10 Cb 82.2 Aa / 95.0 Ba 0.044 Ab / 0.042 Bb
BRSMG Curinga 18.79 Aa / 14.70 Ba 6.28 Ba / 6.99 Ba 0.53 Aa / 0.34 Aa 35.5 Aa / 43.2 Ba 0.068 Ba / 0.053 Ba 3.07 Bb / 1.08 Db 1.93 Bb / 2.19 Bb 0.09 Bb / 0.07 Cb 34.1 Aa / 15.4 Db 0.009 Bb / 0.003 Cb
Carajás 21.90 Aa / 18.63 Aa 5.32 Ca / 8.37 Aa 0.50 Aa / 0.19 Ca 43.8 Aa / 98.1 Ba 0.084 Aa / 0.104 Aa 5.92 Bb / 3.56 Db 1.73 Bb / 2.47 Bb 0.08 Bb / 0.04 Cb 74.0 Aa / 89.0 Ba 0.021 Bb / 0.013 Cb
Casca Branca 21.85 Aa / 19.09 Aa 5.28 Ca / 11.97 Aa 0.50 Aa / 0.25 Ca 43.7 Aa / 76.4 Ba 0.086 Aa / 0.116 Aa 4.91 Bb / 9.02 Cb 1.41 Bb / 5.46 Ab 0.09 Bb / 0.09 Cb 54.6 Aa / 100.2 Ba 0.017 Bb / 0.047 Bb
Cirad 392 24.92 Aa / 21.12 Aa 8.82 Aa / 11.02 Aa 0.47 Aa / 0.18 Ca 53.0 Aa / 117.3 Aa 0.104 Aa / 0.117 Aa 6.01 Bb / 10.22 Bb 2.72 Bb / 5.44 Ab 0.09 Bb / 0.08 Cb 66.8 Aa / 127.8 Aa 0.023 Bb / 0.075 Ab
Comum 17.64 Ba / 14.70 Ba 5.28 Ca / 6.44 Ba 0.46 Aa / 0.19 Ca 38.4 Aa / 77.4 Ba 0.067 Ba / 0.064 Ba 2.39 Bb / 2.52 Db 1.63 Bb / 1.48 Bb 0.07 Bb / 0.03 Cb 34.1 Aa / 84.0 Ba 0.007 Bb / 0.010 Cb
Douradão 14.48 Aa / 16.18 Ba 2.54 Da / 6.63 Ba 0.23 Ba / 0.22 Da 63.0 Aa / 73.6 Aa 0.052 Ba / 0.100 Aa 1.56 Bb / 9.82 Ba 0.97 Bb / 4.36 Aa 0.04 Bb / 0.14 Ba 39.0 Aa / 70.1 Cb 0.004 Bb / 0.073 Aa
Guarani 22.24 Aa / 22.16 Aa 5.90 Ca / 11.08 Aa 0.53 Aa / 0.21 Ca 42.0 Aa / 105.5 Aa 0.085 Aa / 0.151 Aa 8.76 Ab / 1.49 Db 2.50 Bb / 1.72 Bb 0.21 Ab / 0.04 Cb 41.7 Aa / 37.3 Db 0.028 Bb / 0.007 Cb
IRAT 112 20.07 Aa / 23.52 Aa 5.60 Ca / 9.40 Aa 0.69 Aa / 0.40 Aa 29.1 Aa / 58.8 Ba 0.072 Ba / 0.102 Aa 15.67 Ab / 7.85 Cb 3.83 Ab / 2.63 Bb 0.47 Aa / 0.05 Cb 33.3 Aa / 157.0 Aa 0.053 Aa / 0.033 Cb
Moroberekan 11.25 Ba / 13.77 Ba 3.37 Da / 5.50 Ba 0.16 Ba / 0.20 Ca 70.3 Aa / 68.9 Ba 0.046 Ba / 0.061 Ba 1.66 Bb / 4.27 Db 1.26 Bb / 1.63 Bb 0.05 Ba / 0.04 Cb 33.2 Aa / 106.7 Ba 0.004 Bb / 0.018 Cb
Rabo de Burro 16.34 Ba / 13.87 Ba 3.78 Da / 5.57 Ba 0.25 Ba / 0.22 Ca 65.4 Aa / 63.1 Ba 0.061 Ba / 0.058 Ba 1.72 Bb / 3.50 Db 1.21 Bb / 1.44 Bb 0.04 Ba / 0.04 Cb 43.0 Aa / 87.5 Ba 0.005 Bb / 0.013 Cb
Rio Doce 21.18 Aa / 16.79 Ba 5.27 Ca / 8.47 Aa 0.40 Aa / 0.23 Da 53.0 Aa / 73.0 Aa 0.093 Aa / 0.113 Aa 2.38 Bb / 10.60 Ba 1.28 Bb / 5.34 Ab 0.05 Bb / 0.08 Ca 47.6 Aa / 132.5 Aa 0.008 Bb / 0.075 Ab
Saia Velha 11.62 Ba / 15.00 Ba 2.66 Da / 6.29 Ba 0.12 Ba / 0.29 Ba 96.8 Aa / 52.8 Ba 0.041 Ba / 0.053 Ba 1.36 Bb / 1.59 Db 1.21 Bb / 1.44 Bb 0.05 Bb / 0.04 Cb 27.2 Aa / 39.8 Da 0.004 Bb / 0.005 Cb
Tangará 21.81 Aa / 17.89 Aa 7.27 Ba / 7.07 Ba 0.44 Aa / 0.17 Ca 49.6 Aa / 105.2 Aa 0.091 Aa / 0.105 Aa 3.52 Bb / 12.23 Ba 1.92 Bb / 4.86 Aa 0.06 Bb / 0.10 Cb 58.7 Aa / 122.3 Aa 0.009 Bb / 0.082 Aa
Três Meses Branco 23.26 Aa / 23.40 Aa 6.56 Ba / 8.35 Aa 0.49 Aa / 0.31 Ba 47.5 Aa / 75.5 Ba 0.093 Aa / 0.110 Aa 16.81 Ab / 13.44 Bb 4.39 Ab / 5.02 Ab 0.29 Aa / 0.14 Bb 58.0 Aa / 96.0 Ba 0.064 Aa / 0.071 Ab
Genotypes Phase III
2015 / 2017
Irrigated Stressed
A E gs WUE CE A E gs WUE CE
Agulhão 19.14 Aa / 19.18 Ba 5.82 Aa / 5.65 Ca 0.42 Aa / 0.37 Ca 45.6 Aa / 51.8 Ea 0.066 Ba / 0.067 Ca 8.26 Bb / 11.68 Ab 2.53 Bb / 4.64 Aa 0.11 Ab / 0.23 Ab 75.1 Aa / 50.8Ea 0.031Bb / 0.039 Cb
Aimoré 21.90 Aa / 18.78 Ba 7.25 Aa / 7.27 Ba 0.50 Aa / 0.19 Da 43.8 Aa / 98.8 Ba 0.085 Aa / 0.115 Ba 14.07 Ab / 8.94 Bb 3.93 Ab / 3.41 Bb 0.21 Ab / 0.07 Cb 67.0 Aa / 127.7 Ab 0.061 Aa / 0.058 Bb
Amarelão 21.05 Aa / 13.74 Ca 6.86 Aa / 10.65 Aa 0.25 Ca / 0.14 Ea 84.2 Aa / 98.1 Ba 0.090 Aa / 0.075 Ca 7.04 Bb / 5.05 Cb 2.68 Bb / 5.03 Ab 0.07 Ab / 0.07 Cb 100.6 Aa / 72.3 Cb 0.029 Bb / 0.024 Cb
Arroz 4 meses 20.10 Aa / 23.49 Aa 5.89 Aa / 7.49 Ba 0.44 Aa / 0.32 Ca 45.7 Aa / 73.4 Ca 0.081 Aa / 0.106 Ba 8.68 Bb / 10.39 Bb 2.62 Bb / 3.44 Bb 0.12 Ab / 0.10 Cb 7 2.3 Aa / 103.9 Ab 0.038 Bb / 0.058 Bb
Arroz Carolino 22.48 Aa / 18.76 Ba 6.91 Aa / 7.47 Ba 0.46 Aa / 0.23 Da 48.9 Aa / 81.6 Ca 0.089 Aa / 0.093 Ba 9.65 Bb / 13.91 Ab 3.23 Ab / 4.70 Ab 0.14 Ab / 0.11 Cb 7 4.9 Aa / 126.5 Ab 0.041 Bb / 0.091 Aa
Bico Ganga 19.23 Aa / 15.79 Ca 7.28 Aa / 8.16 Ba 0.29 Ba / 0.23 Da 66.3 Aa / 68.7 Da 0.074 Aa / 0.069 Ca 5.94 Bb / 9.30 Bb 2.77 Bb / 3.91 Bb 0.07 Ab / 0.09 Cb 84.9 Aa / 103.3 Ab 0.022 Bb / 0.047 Ca
Branquinho 90 Dias 17.46 Aa / 16.18 Ca 5.47 Aa / 5.40 Ca 0.49 Aa / 0.15 Ea 35.6 Aa / 107.9 Aa 0.060 Ba / 0.090 Ba 13.80 Ab / 12.67 Aa 3.55 Ab / 3.66 Bb 0.24 Ab / 0.11 Ca 57.5 Aa / 115.2 Aa 0.056 Aa / 0.072 Aa
BRS Esmeralda 20.40 Aa / 16.09 Ca 6.76 Aa / 5.89 Ca 0.44 Aa / 0.33 Ca 46.4 Aa / 48.9 Ea 0.073 Aa / 0.060 Da 8.46 Bb / 9.16 Bb 3.25 Ab / 4.54 Aa 0.13 Ab / 0.14 Cb 65.1 Aa / 65.4 Db 0.030 Bb / 0.037 Cb
BRS Primavera 21.65 Aa / 23.55 Ca 8.15 Aa / 10.82 Aa 0.34 Ba / 0.31 Ca 63.7 Aa / 76.0 Ca 0.085 Aa / 0.112 Ba 6.84 Bb / 9.63 Bb 2.89 Bb / 5.69 Ab 0.08 Ab / 0.08 Cb 85.5 Aa / 120.4 Ab 0.027 Bb / 0.044 Cb
BRS Serra Dourada 21.22 Aa / 21.41 Ba 8.28 Aa / 7.45 Ba 0.34 Ba / 0.35 Ca 62.4 Aa / 61.2 Da 0.082 Aa / 0.093 Ba 9.27 Bb / 12.52 Ab 3.39 Ab / 4.39 Ab 0.09 Ab / 0.16 Bb 103.0 Aa / 78.3 Cb 0.040 Bb / 0.060 Bb
BRS Soberana 24.50 Aa / 26.51 Ca 8.09 Aa / 8.49 Aa 0.52 Aa / 0.58 Aa 47.1 Aa / 45.7 Ea 0.100 Aa / 0.090 Ba 16.46 Ab / 16.71 Ab 5.01 Ab / 5.52 Ab 0.24 Ab / 0.27 Ab 68.6 Aa / 61.9 Db 0.074 Aa / 0.061 Bb
BRSMG Curinga 16.94 Aa / 24.10 Ca 6.68 Aa / 10.04 Aa 0.36 Ba / 0.43 Ba 47.1 Aa / 56.1 Ea 0.060 Ba / 0.102 Ba 5.19 Bb / 7.53 Bb 2.32 Bb / 3.46 Bb 0.08 Ab / 0.10 Cb 64.9 Aa / 75.3 Cb 0.018 Bb / 0.032 Cb
Carajás 21.07 Aa / 19.95 Ba 6.78 Aa / 7.43 Ba 0.41 Aa / 0.29 Ca 51.4 Aa / 68.8 Da 0.091 Aa / 0.084 Ca 7.37 Bb / 11.73 Ab 2.46 Bb / 4.76 Ab 0.09 Ab / 0.14 Cb 81.9 Aa / 83.8 Ca 0.034 Bb / 0.053 Cb
Casca Branca 18.03 Aa / 21.42 Ba 6.10 Aa / 9.33 Aa 0.36 Ba / 0.28 Ca 50.1 Aa / 76.5 Cb 0.075 Aa / 0.106 Ba 10.47 Bb / 10.29 Bb 3.51 Ab / 4.15 Bb 0.14 Ab / 0.09 Cb 74.8 Aa / 114.3 Aa 0.048 Ab / 0.064 Bb
Cirad 392 21.40 Aa / 26.83 Ca 7.27 Aa / 9.99 Aa 0.46 Aa / 0.34 Ca 46.5 Aa / 78.9 Ca 0.084 Aa / 0.141 Aa 10.71 Bb / 14.63 Ab 3.48 Aa / 6.00 Ab 0.15 Ab / 0.17 Bb 71.4 Aa / 86.1 Ca 0.047 Ab / 0.082 Ab
Comum 19.4 5 Aa / 12.64 Ca 7.28 Aa / 6.90 Ba 0.46 Aa / 0.14 Ea 42.3 Aa / 90.3 Ba 0.081 Aa / 0.067 Ca 9.33 Bb / 6.72 Cb 3.11 Bb / 4.75 Ab 0.09 Bb / 0.07 Cb 103.7 Aa / 96.0 Ba 0.042 Bb / 0.036 Cb
Douradão 22.37 Aa / 18.30 Ba 3.07 Ba / 7.34 Ba 0.41 Ca / 0.21 Da 54.6 Aa / 87.1 Ba 0.064 Ba / 0.093 Ba 12.67 Ab / 10.25 Bb 2.85 Ba / 4.17 Bb 0.13 Ab / 0.11 Cb 97.5 Aa / 93.2 Ba 0.042 Ba / 0.058 Bb
Guarani 20.76 Aa / 19.00 Ba 7.02 Aa / 8.20 Ba 0.41 Aa / 0.16 Ea 50.6 Aa / 118.8 Aa 0.087 Aa / 0.123 Aa 11.61 Ab / 3.25 Cb 3.74 Ab / 2.25 Cb 0.15 Ab / 0.03 Cb 77.4 Aa / 108.3 Aa 0.054 Ab / 0.016 Ca
IRAT 112 24.93 Aa / 19.59 Ba 6.90 Aa / 6.86 Ba 0.60 Aa / 0.29 Ca 41.6 Aa / 67.6 Db 0.097 Aa / 0.081 Ca 14.29 Ab / 18.02 Ab 3.76 Ab / 5.58 Aa 0.22 Ab / 0.21 Ab 65.0 Aa / 85.8 Ca 0.064 Ab / 0.086 Aa
Moroberekan 11.73 Aa / 12.81 Ca 3.13 Ba / 4.63 Ca 0.13 Ca / 0.25 Da 90.2 Aa / 51.2 Eb 0.043 Ba / 0.046 Da 6.14 Bb / 7.77 Bb 1.86 Bb / 2.87 Bb 0.11 Aa / 0.11 Cb 55.8 Aa / 70.6 Ca 0.021 Ba / 0.032 Ca
Rabo de Burro 18.68 Aa / 13.07 Ca 4.99 Ba / 5.42 Ca 0.32 Ba / 0.33 Ca 58.4 Aa / 39.6 Ea 0.058 Ba / 0.044 Da 6.88 Bb / 12.99 Aa 1.99 Ba / 4.77 Aa 0.12 Ab / 0.26 Aa 57.3 Aa / 50.0 Ea 0.020 Bb / 0.047 Ca
Rio Doce 21.50 Aa / 23.47 Aa 6.78 Aa / 9.90 Aa 0.42 Aa / 0.29 Ca 51.2 Aa / 80.9 Cb 0.045 Aa / 0.133 Aa 6.04 Bb / 14.43 Ab 2.29 Bb / 5.57 Ab 0.08 Ab / 0.12 Cb 75.5 Aa / 120.2 Aa 0.027 Bb / 0.102 Ab
Saia Velha 15.82 Aa / 13.16 Ca 3.49 Ba / 6.81 Ba 0.22 Ca / 0.29 Ca 71.9 Aa / 45.4 Eb 0.054 Ba / 0.046 Da 5.90 Bb / 5.43 Cb 1.65 Bb / 2.72 Bb 0.07 Ab / 0.09 Cb 84.3 Aa / 60.3 Da 0.017 Bb / 0.019 Ca
Tangará 21.27 Aa / 18.98 Ba 6.88 Aa / 8.02 Ba 0.47 Aa / 0.23 Da 45.3 Aa / 82.5 Cb 0.061 Aa / 0.100 Ba 10.10 Bb / 9.19 Bb 3.64 Ab / 3.52 Bb 0.18 Ab / 0.09 Cb 56.1 Aa / 102.1 Aa 0.038 Bb / 0.050 Cb
Três Meses Branco 22.42 Aa / 25.18 Aa 6.81 Aa / 9.74 Aa 0.56 Aa / 0.34 Ca 40.0 Aa / 74.1 Ca 0.083 Aa / 0.125 Aa 15.98 Aa / 15.14 Ab 4.25 Ab / 5.54 Ab 0.25 Ab / 0.16 Bb 61.6 Aa / 94.6 Bb 0.066 Aa / 0.080 Ab

Phase I: Means followed by the same capital letter in the column do not differ by the Scott-Knott test at 5 % error probability. Transformed data in square root of Y+1.0SQRT (Y+1.0) for the statistical analysis; Phase II and Phase III: capital letters compare genotypes within each water regime and small letters compare water regimes within each genotype. Means followed by the same capital letter in the column and means followed by the same letter on the rows do not differ by the Scott-Knott test at 5 % error probability. Transformed data in square root of Y+1.0SQRT (Y+1.0) for the statistical analysis.

When water deficits start to increase, leaf stomatal conductance usually decreases faster than carbon assimilation, leading to increased WUE. The WUE reflects the multiple environmental stimuli perceived and the capacity of a particular genotype to sense the onset of changes in moisture availability and therefore to fine-tune its water status in response to the environment (Wilkinson, 2004; Blankenagel et al., 2018).

However, despite the negative impact of water deficit on gas exchange, in both years of trials, Bico Ganga, BRS Esmeralda, BRSMG Curinga, and Guarani (top genotypes) improved their WUE (44 %) when compared with optimal irrigation conditions. This was most probably due to higher stomatal control efficiency, keeping approximately 40 % of the photosynthetic process and drastically reducing stomatal conductance (70 %) by closing the stomata process. Although Rabo de Burro did not show increase in WUE, it presented a recovery of the gas exchange apparatus compared to irrigated plants, which can be justified partly by its vigorous root system.

In addition to increased relative stomatal limitation, drought stress is responsible for reducing maximum Rubisco carboxylation activity and electron transport and therefore ribulose bisphosphate (RuBP) regeneration (Perdomo et al., 2017). The carboxylation efficiency could be considered an estimate of the Rubisco activity, illustrating its limitations under stress conditions (Niinemets et al., 2009). In our study, all upland rice genotypes showed a poor capacity to overcome limitation in CO2 diffusion by stomata and mesophyll and effective CO2 fixation (70 % of CE reduction) during phase II for both years of trials. After replenishing 50 % of water at the column base for 10 days, recovery of 55 % and 64 % in the carboxylation efficiency was observed in 2015 and 2017, respectively. Considerable loss of Rubisco activity during stress conditions were also reported for sugarcane subjected to water deficit (Saliendra et al., 1996; Vu and Allen Jr., 2009). Overall, a response pattern was not observed among genotypes with greater yield performance under water deficit, since they showed divergent physiological responses of gas exchange.

Furthermore, remobilization of photoassimilates from vegetative into reproductive structures may have a significant effect on grain yield, although this component was not evaluated in our study. As demonstrated for cereals (Blum et al., 1994) and legumes (Chaves et al., 2002), nutrient pre-anthesis reserves are used for grain filling in addition to current assimilates. In rice, drought-induced leaf senescence also promotes assimilate allocation to grains under development, shortening grain filling and increasing the grain filling rate (Sehgal et al., 2018). Moreover, senescence and reserve mobilization are integral components of plant development and basic strategies in stress mitigation (Lemoine et al., 2013).

Water stress effects on Ψw, RWC, Ψs, and OA, evaluated only in the 2015 trial, are shown in Table 6. Among top genotypes, BRS Esmeralda, BRSMG Curinga, Guarani, and Rabo de Burro showed a more pronounced gradient of ψw and probably enhanced water absorption capacity. Besides, advance of the most severe internal damage may have reduced in the reproductive organs under the drought period. Conversely, Bico Ganga kept high water potential during the water deficit period, which may be associated to a more robust root system in the second soil layer and thus higher panicle water potential, which probably contributes to increased grain yield. According to Guimarães et al. (2016), plants that prevent dehydration presented higher water potential and earliness in flowering, lower height, lower leaf area or lower tillering. Regarding the trait RWC, which is directly related to the plant water status, values ranged from ∼ 82 % in leaves under irrigated condition to 75 % for stressed plants. On the other hand, BRSMG Curinga presented significant RWC reduction due to the stress imposed. This divergent responses regarding leaf water status suggest greater capacity of top genotypes to save water during drought and stimulate an adjustment of the photosynthetic capacity to tolerate changes in water availability (Silva et al., 2007; Rodrigues et al., 2009; Graça et al., 2010). The mechanism of osmotic adjustment (OA), usually accomplished by accumulation of compatible solutes (ψs) and maintenance of RWC, although significant for all genotypes, was numerically higher for BRS Esmeralda, followed by Bico Ganga and Guarani, compared to BRSMG Curinga and Rabo de Burro (top genotypes). This mechanism in upland rice plants during the reproductive phase allows maintenance of adequate physiological state, in which the leaves remain green and cool for a longer time, besides allowing the establishment and retention of spikelet and, consequently, grain yield sustenance (Fischer et al., 2003).

Table 6 Water potential (Ψw, MPa), osmotic potential (Ψs, MPa), relative water content (RWC, %), and osmotic adjustment (OA; MPa) of upland rice (Oryza sativa L.) grown under irrigated and drought conditions. Trial in 2015. 

Genotypes Water level
Irrigated Stressed
Ψw Ψs RWC OA Ψw Ψs RWC OA
Agulhão –0.39 Aa –1.235 Ba 81.73 Ba 0.000 Aa –0.95 Ab –1.272 Ca 70.09 Bb 0.037 Ea
Aimoré –0.16 Ba –0.939 Ea 80.65 Ba 0.000 Aa –0.53 Ba –1.062 Da 76.64 Aa 0.122 Db
Amarelão –0.28 Aa –1.080 Da 79.67 Ba 0.000 Aa –0.36 Ba –1.210 Cb 68.55 Bb 0.130 Db
Arroz 4 meses –0.03 Ba –1.079 Da 81.19 Ba 0.000 Aa –0.90 Ab –1.132 Aa 70.03 Bb 0.050 Ea
Arroz Carolino –0.02 Ba –0.987 Ea 79.34 Ba 0.000 Aa –0.55 Bb –1.205 Cb 75.62 Aa 0.217 Bb
Bico Ganga –0.20 Ba –1.053 Da 76.19 Ba 0.000 Aa –0.38 Ba –1.255 Cb 73.98 Ba 0.202 Bb
Branquinho 90 Dias –0.03 Ba –0.940 Ea 84.57 Ba 0.000 Aa –0.39 Ba –1.206 Cb 76.99 Ab 0.266 Ab
BRS Esmeralda –0.02 Ba –1.250 Ba 83.21 Ba 0.000 Aa –1.12 Ab –1.495 Ab 79.36 Aa 0.245 Ab
BRS Primavera –0.24 Aa –1.141 Ca 86.35 Ba 0.000 Aa –0.48 Ba –1.399 Ab 83.78 Aa 0.258 Ab
BRS Serra Dourada –0.33 Aa –1.138 Ca 79.42 Ba 0.000 Aa –0.38 Ba –1.267 Cb 77.56 Aa 0.129 Db
BRS Soberana –0.35 Aa –1.115 Ca 76.12 Ba 0.000 Aa –0.36 Ba –1.165 Ca 66.89 Bb 0.116 Db
BRSMG Curinga –0.12 Ba –1.218 Ba 83.04 Ba 0.000 Aa –0.93 Ab –1.235 Ca 73.81 Bb 0.022 Ea
Carajás –0.03 Ba –0.995 Da 79.01 Ba 0.000 Aa –0.40 Ba –1.216 Cb 72.64 Ba 0.221 Bb
Casca Branca –0.03 Ba –1.403 Aa 96.72 Aa 0.000 Aa –0.49 Bb –1.446 Aa 76.48 Ab 0.043 Eb
Cirad 392 –0.02 Ba –1.057 Da 76.17 Ba 0.000 Aa –0.39 Ba –1.172 Ca 72.22 Ba 0.114 Db
Comum –0.04 Ba –1.522 Ab 77.94 Ba 0.000 Aa –0.51 CB –1.783 Aa 69.88 Bb 0.051 Ea
Douradão –0.45 Aa –1.130 Ca 83.08 Ba 0.000 Aa –0.71 Ba –1.142 Da 78.11 Aa 0.012 Eb
Guarani –0.03 Ba –1.163 Ca 81.59 Ba 0.000 Aa –0.43 Bb –1.318 Bb 79.39 Aa 0.155 Cb
IRAT 112 –0.04 Ba –0.916 Ea 80.78 Ba 0.000 Aa –0.50 Bb –1.017 Da 71.00 Bb 0.101 Db
Moroberekan –0.12 Ba –1.259 Ba 83.83 Ba 0.000 Aa –1.44 Ab –1.325 Ba 75.88 Ab 0.035 Ea
Rabo de Burro –0.46 Aa –1.212 Ba 82.30 Ba 0.000 Aa –1.33 Ab –1.228 Ca 81.19 Aa 0.016 Ea
Rio Doce –0.04 Ba –1.080 Da 79.49 Ba 0.000 Aa –0.63 Bb –1.321 Bb 74.35 Ba 0.241 Ab
Saia Velha –0.51 Aa –1.065 Da 79.35 Ba 0.000 Aa –1.23 Ab –1.178 Ca 70.34 Bb 0.113 Db
Tangará –0.40 Aa –0.988 Ea 70.98 Ba 0.000 Aa –0.42 Ba –1.146 Db 70.69 Ba 0.160 Cb
Três Meses Branco –0.28 Aa –0.918 Ea 79.71 Ba 0.000 Aa –0.73 Bb –1.115 Cb 73.69 Ba 0.316 Ab

Capital letters compare genotypes within each water regime and small letters compare water regimes within each genotype. Means followed by the same capital letter in the column and means followed by the same letter on the rows do not differ by the Scott-Knott test 5 % error probability. Transformed data in square root of Y+1.0SQRT (Y+1.0) for the statistical analysis.

This study describes important aspects of drought-induced effect on upland rice, providing a better understanding of morphophysiological changes under water deficit. Top genotypes showed distinct strategies by activating different physiological responses: higher ability to save water on leaves (Bico Ganga, BRS Esmeralda, BRSMG Curinga and Rabo de Burro), lower leaf water potential (Bico Ganga, BRS Esmeralda, BRSMG Curinga and Guarani), higher ability to reduce vegetative structures (Bico Ganga, BRSMG Curinga and Rabo de Burro), higher efficiency in the use of water (Bico Ganga, BRS Esmeralda, BRSMG Curinga and Guarani), higher photosynthetic capacity (Guarani), and improved ability to absorb water from drying soil, either by osmotic adjustment (Bico Ganga, BRS Esmeralda and Guarani) or additional investment in the root system (BRSMG Curinga and Rabo de Burro). Therefore, different mechanisms, such as vegetative morphology, gas exchange, water status, and root system could be explored simultaneously to support the development of drought-tolerant rice cultivars by breeding programs.

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Received: December 13, 2019; Accepted: April 03, 2020

*Corresponding author <anna.lanna@embrapa.br>

Edited by: Leonardo Oliveira Medici

Authors’ Contributions

Conceptualization: Vianello, R.P.; Lanna, A.C.; Brondani, C. Data analysis: Lanna, A.C.; Coelho, G.R.C.; Moreira, A.S.; Terra, T.G.R. Data acquisition: Lanna, A.C.; Coelho, G.R.C.; Saraiva, G.R.; Lemos, F.S. Design of methodology: Lanna, A.C.; Guimarães, P.H.R.; Morais Júnior, O.P. Writing and editing: Lanna, A.C.; Moreira, A.S.; Brondani, C.; Vianello, R.P.

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