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J Plant Biotechnol (2024) 51:063-070

Published online March 28, 2024

https://doi.org/10.5010/JPB.2024.51.007.063

© The Korean Society of Plant Biotechnology

Effects of flooding conditions and phytohormones on coleoptile elongation in Indica rice varieties

Khac Nhu Nghi ・Ngoc Ai Trinh

The Institute of Biotechnology, Tra Vinh University, Tra Vinh 87000, Vietnam

Correspondence to : e-mail: nknhu@tvu.edu.vn

Received: 9 March 2024; Revised: 20 March 2024; Accepted: 20 March 2024; Published: 28 March 2024.

This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

The unpredictable scenarios of current climate change pose great challenges for global food security. Climate change triggers submergence, a natural disaster that affects cereal production in the Mekong Delta of Vietnam. Among cereals, rice is a unique species in its ability to germinate and develop a long coleoptile under water. Several previous studies indicated that the capacity of japonica rice is better than indica rice cultivars. Herein, we assessed the ability of coleoptile elongation and the role of exogenous auxin (IAA) in promoting rice coleoptile length under dark, flooded conditions using 20 indica rice varieties collected from the Mekong Delta. We germinated 20 rice seeds per variety under water (with and without adding auxin at different concentrations) for several days and measured the coleoptile length at two different timepoints of submergence. We found that the ability to develop a long coleoptile under water was not related to the rice subspecies. The average coleoptile length at day 8 and the growth curve from the beginning to day 8 of the submergence experiment of our rice cultivars were the same. We also found that 10 μM of IAA concentration expressed a significant effect on the capacity of coleoptile elongation in both long and short coleoptile-harboring indica rice subspecies. Our results suggested that OM108, OM5451, and ĐT8 are promising rice cultivars for rice production in the Mekong Delta of Vietnam.

Keywords submergence, rice (Oryza sativa L.), auxin, climate change, rice coleoptile

Climate change is a negative shift in global climate patterns. It resulted in global warming as well as the increase of extreme weather-related events such as flooding, drought, salinity; wildfire and much more (Arora 2019; Nielsen-Gammon et al. 2020; Seppelt et al. 2022). They impacted directly or indirectly to the livelihood of billions of people over the world, of which there are million global farmers (Arivelarasan et al. 2023; FAO, IFAD, UNICEF, WFP, WHO 2020; Raj et al. 2022). Flooding is one of the most significant challenges for crop production. In a period of 10 years (from 2006 to 2016), it was the reason for almost 70% yield loss of different crops on a global scale (FAO 2018; Patel et al. 2014). Recent studies indicate that there is more than 17 million km2 of global agricultural land affected and billions US dollars lost due to flooded water yearly (Kaur et al. 2020; Vaidya et al. 2024; Voesenek and Sasidharan 2013). The flood predicted areas of agricultural land could grow rapidly in the end of this century, especially in Southeast Asia and India (Coumou and Rahmstorf 2012; Lan et al. 2024).

Currently, feeding more than 8 billion people on the planet is a big challenge for global food production although more than food has been produced during the last decades (Fróna et al. 2019; Strzyżyńska 2022). Among the cereal crops, rice plays an extremely important role in ensuring food security. It is the third leading crop in harvested area and production as well (FAO 2022). Rice is a crucial food supply for more than half of the global population with over 90% of rice cultivated and consumed in Asian countries (Bao 2023; Fukagawa and Ziska 2019; Yu et al. 2021).

Rice is the unique cereal which can germinate in both flooded and anoxic environments (Wu and Yang 2020). Rice is special in ability to create and elongate the coleoptile beyond the water surface in submergence condition in a few days (Miro and Ismail 2013; Yu et al. 2021). However,

rice production is affected seriously by flooding because about one-third of areas used for rice cultivation is usually low and has an annual submerged tendency (Muthayya et al. 2014; Su and Kuo 2023). Millions of hectares of rice-cultivated area were affected with millions of tons of rice lost yearly in the Asia region due to flooding (GriSP 2013; Su and Kuo 2023).

The anaerobic germination tolerance of rice was presented at elongation ability of coleoptiles under flooded water. This ability of rice cultivars is regulated by both division and elongation capacity of cells, with the latter being the major in rice as well as other monocot (Zhang et al. 2021). Cell division plays an important role at the first phase of anaerobic germination, then cell elongation occurs and goes on until the tip of the coleoptile reaches the surface of flooded water.

The certain role of phytohormone in plant response to abiotic stresses such as drought, saltwater intrusion, flooding was well-known (Khan et al. 2012; Zheng et al. 2023). Beside ethylene and gibberellin, auxin (IAA) is the most plentiful hormone which contributed to the growth and development of plant (Gallei et al. 2020; Sosnowski et al. 2023; Vanneste and Friml 2009). Many studies have indicated that IAA plays a key role in improving the germination ability as well as seedling establishment of rice seed under water by stimulating the coleoptile elongation (Lee et al. 2023; Lu et al. 2023; Nghi et al. 2021; Wu and Yang 2020). Nghi et al. (2021) approved that adding directly IAA (10 µM) into the experimental water under dark submergence increased the coleoptile length of japonica rice varieties; whereas, the experimental results of Lee et al. (2023) suggested the high concentration of endogenous auxin enhanced the elongation of coleoptile and repressed the growth of root and the appearance of the first leaf of japonica rice during germination under completely dark submergence. Accumulation of IAA stimulated the coleoptile elongation of japonica rice and the scale is dependent on the rice genotypes (Lee et al. 2023; Nghi et al. 2021; Wu and Yang 2020). Over 500 thousand rice accessions are collected in the global gene bank (Vieira et al. 2022); and although many researches to identify the role of auxin in regulating ability of anaerobic germination tolerance of rice varieties were conducted, the results are still under debate.

In our present study, we assess the ability of coleoptile elongation as well as the role of exogenous IAA in promoting the coleoptile length of indica rice cultivars under dark flooded conditions. These varieties are commonly cultivated rice cultivars in the Mekong delta region of Vietnam. The results indicate that the difference in exogenous auxin concentration and rice genotype determine the final length of both short and long-coleoptile indica rice varieties.

Plant material

All 20 rice cultivars used in this study belonged to indica rice subgroup of Oryza sativa L. They were obtained from Cuu Long delta rice research institute and other areas of Mekong rice production region. They widely adapted to the local soil and climatic conditions. Most of them are OM rice accessions which are being popular planted in the fields at Mekong delta. The collected rice seeds were stored in a cold room at 4°C to use for the long term.

Seed germination under dark submergence

The phenotyping experiment was conducted as previously described (Nghi et al. 2019). The rice seed coat was removed and sterilized the surface with 70% ethanol and 3% sodium hypochlorite for 1 min and 15 min; respectively. Then, sterile water was used for washing 3 times after treating ethanol and 5 times after treating sodium hypochlorite. The intact sterile seeds were put on the bottom of magenta boxes where they were covered with a thin layer of sterile cotton. This box was filled with sterile water. The seeds were allowed to germinate at 30°C in the dark submerged condition for 4 and 8 days. 20 seeds of each rice variety were utilized per each experiment and all experiments were repeated 2 times. The coleoptile length at two different time points, then, would be measured using electron digital calipers. The coleoptile samples of rice varieties would be collected and stored to use for subsequent studies.

Auxin experiment

Six rice varieties which were representative of shortest (JASMINE 85, OM4900, OM6976) and longest (ĐT8, OM5451, OM108) coleoptile group at day 8 of submergence (SUB 8D) were selected for the treatments. The rice seeds were treated as described in the above experiments. Each experiment was performed using 20 rice grains. Rice germination occurred in the completely dark submergence and IAA was supplemented directly inside the water environment at day 2 of submergence. The added amount of IAA was calculated in order to ensure the final concentration of the treated environment were 1 µM and 10 µM. At day 8 of submergence, the coleoptile length of the controls and treatments (1 µM and 10 µM) was assessed using electron digital calipers.

Data analysis

We analyzed all data obtained from experiments using statistical program R and Excel software.

The greatly variation in coleoptile elongation ability of indica rice cultivars under submergence

In this experiment, the anaerobic germination ability of 20 indica rice accessions was analyzed through measuring their coleoptile length in different time points (4 days (SUB 4D) and 8 days (SUB 8D) after submergence) under absolutely dark and submergence condition (Fig. 1A). We identified a significant difference in coleoptile length in both SUB 4D and SUB 8D among rice cultivars (Fig. 1A and Table 1). The coleoptile length of rice cultivars of SUB 4D is ranged from 0.95 to 3.11 cm, with a mean value of 1.87 cm; while these data of SUB 8D is from 2.88 to 6.94 cm, with a mean value of 5.11cm (Fig. 1A and Table 1). The CV value of SUB 4D and SUB 8D was 0.35 and 0.21, respectively, indicating that the variation of coleoptile length of SUB 4D was larger (Table 1).

Fig. 1. (A) Coleoptile length at days 4 and 8 of submergence of 20 indica rice varieties. (B) Box plot of coleoptile length at days 4 and 8 of submergence among the OM rice group and other rice groups. Values represent the mean ± SD. Student’s t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001

Table 1 Statistical analysis of traits related to coleoptile length in rice varieties

TraitMeanSDSERangeCV
Average at Day 4 (mm)18.76.51.59.5–31.10.35
Average at Day 8 (mm)51.110.52.328.8–69.40.21
75th percentile at Day 8 (mm)54.210.72.432.1–74.70.2
Ratio Day 8/43.01.10.21.4–5.70.4


The coleoptile elongation tendency under flooded water of these indica rice cultivars is unstable in 2 different time points under complete dark submergence. While variety CL309 and OM 6976 always belong to longest and shortest coleoptile groups, respectively, at both day 4 and day 8 after submergence; ST23 and OM576 rice cultivars indicated the contrary trend in 2 different time points. ST23 is located in the longest group at day 4 and shortest group at day 8, whereas the variety OM576 is vice versa. The coleoptile of OM5451 and OM108 is medial at first 4 days of submergence, but their coleoptile elongation ability was strong and displayed very long coleoptile after next 4 days of submergence (Fig. 1A).

The difference in coleoptile length between OM rice group and the other on 4th day of submergence

An analysis of the difference in coleoptile length among rice accessions at day 4 and day 8 of submergence was conducted. We divided these rice varieties into two groups (OM group and other) and analyzed the coleoptile length variation between them at 2 time points of experiment. The results indicated that the coleoptile which was developed from accessions of OM group of SUB 4D is significantly shorter than the other, whereas there is no significant difference in coleoptile length observed between two groups of SUB 8D (Fig. 1B). In our results, the rice varieties OM108 and OM576 (belonged to OM group) showed the longest coleoptile lengths at SUB 8D (Fig. 1A).

The coleoptile growth speed of the collected indica rice accessions

We selected two subgroup of rice varieties (three varieties per each), which developed the longest and shortest coleoptile in length at SUB 8D, to identify the developmental tendency and the growth rate (displayed by the trait ratio 8D/4D) of their coleoptile from day 1 to day 8 under dark submergence (Fig. 2A, E). The analyzed result indicated that the elongation speed is different between not only selected rice of 2 subgroups but also in whole our indica rice accessions (Fig. 2B). The growth curve of these selected subgroups showed the rate of coleoptile elongation is relatively slow from day 0 to 4 of submergence; reach an exponential growth between 4 and 6 days; slow down and go to the plateau stage from day 7 to 8 of submergence (Fig. 2C, D).

Fig. 2. (A) The average length of long (OM108, OM5451, and ĐT8) and short coleoptile (JASMINE85, OM6976, and OM4900) rice variety groups at days 4 and 8 of submergence (mean ± SD). Student's t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001. (B) The ratio between SUB 8D and SUB 4D of coleoptile length of indica rice accessions. (C and D) Growth curve of coleoptile length from days 0-8 of long and short coleoptile rice variety groups under dark submergence (mean ± SD). Student’s t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001. (E) Coleoptile length SUB 8D of six chosen rice varieties.

The effect of IAA (auxin) on elongation of rice coleoptile under submergence

In order to understand the IAA role in determining the final length of rice coleoptile after 8 days of germination under submergence, we conducted other experiments using the same of two above subgroups of rice varieties. IAA was utilized in the experiments with two different concentrations (1 µM and 10 µM). We found that IAA addition in experimental water impacted the coleoptile elongation ability of rice cultivar. The scale depends on IAA concentration and kind of rice accession (Fig. 3).

Fig. 3. (A) Influence of IAA (1 µM) treatment at day 2 on the final coleoptile length of long and short coleoptile rice variety groups under dark submergence (mean ± SD). (B) Influence of IAA (10 µM) treatment at day 2 on the final coleoptile length of long and short coleoptile rice variety groups under dark submergence (mean ± SD). (C) Coleoptile length between control and treatment of JASMINE85 and ĐT8 rice varieties. Values represent the mean ± SD. Student’s t-test: Not statistically (ns) significant (P > 0.05); statistically significant (P ≤ 0.05). Lowercase letters indicate significant differences among treatments.

In the first IAA experiment, we tried with 1 µM of IAA. The result indicated that, in general, there is a significant variation in coleoptile length between the control and treatment of two subgroups at SUB 8D. But If we go in detail, only the OM4900 (representative of the shortest group) and OM108 (representative of the longest group) displayed the great difference (Fig. 3A). Whereas, adding IAA at 10 µM of concentration showed a positive influence on the final length of coleoptile in whole rice varieties used in the experiment (Fig. 3B, C). The coleoptile length of the treatment is much longer than the control one at SUB 8D (Fig. 3B, C).

Because of the shortage of fresh water and labor resources as well as the increase of input cost, direct seeding became a major method for rice production (Aung et al. 2023; Miro and Ismail 2013) and the ability of rice cultivars to develop a long coleoptile under flooded water is significant. Many previous studies indicated that this ability of japonica rice varieties was better than indica one (Aung et al. 2023; Nghi et al. 2019; Su et al. 2021; Zhang et al. 2017). However, our results showed a high coleoptile elongation capacity of indica accession. Our indica group could develop a long coleoptile with the average length was even the same to japonica group of Nghi et al. (2019) at Day 8 of dark submergence at 30°C (5.11 cm in comparison with 5.15 cm) (Table 1).

Mekong delta is the biggest region for rice production in Vietnam. It makes up over 50% of harvested area and 60% of rice productivity of Vietnam (Vietnam general statistics office 2021). Among rice cultivars which are generally cultivating in this delta, OM rice varieties are in the majority. These rice cultivars were developed from Cuu Long delta rice research institute of Vietnam. Therefore, we decided to divide our indica rice accessions into two group are OM group and other group. In our studies, the rice varieties OM108 and OM576 which showed the longest coleoptile lengths SUB 8D belonged to OM group (Fig. 1a). OM rice varieties are commonly cultivated rice varieties at Mekong delta region of Vietnam because they were bred over several generations to widely adapt to cultivation strategy of direct seeding and different agroecosystems in this area (Le and Umetsu 2022). Therefore, the ability of developing a long coleoptile under submergence is a crucial property.

The difference of coleoptile length between 2 time points of submergence of each rice variety in our indica rice panel was significant. Some varieties such as OM576, OM5451 developed coleoptiles to be among shortest and medium groups at SUB 4D; whereas at SUB 8D their coleoptile length belonged to the longest one (Fig. 1A). There are several factors affecting this property. Many previous studies revealed that several genes in rice related to extension of anaerobic germination ability show a significantly different expression level in different time points of germination stage of rice seed (He et al. 2023; Magneschi et al. 2009; Nghi et al. 2019; Su et al. 2021; Zhang et al. 2017).

The coleoptile length of each rice variety depends on their elongation rate under water. In our study, the selected rice varieties between two subgroups created coleoptiles with significant difference in length at SUB 8D. Analyzing the growth model of coleoptile between our two subgroups indicated that the difference in coleoptile length from the beginning to day 3th of germination is not really great; the elongation rate began to become significantly different from day 4th and reach greatest and stable at day 7th and later of germination (Fig. 2C, D). Several previous researches in japonica rice also displayed the same pattern as our study (He et al. 2023; Magneschi et al. 2009; Nghi et al. 2019). It suggests that the coleoptile growth pattern is the same for both indica and japonica rice cultivars which showed the ability of anaerobic germination tolerance. The variation in coleoptile elongation rate decided their final length.

Auxin (IAA) is a phytohormone which has the crucial role in promoting the growth of tip parts of the plant through stimulating cell wall enlargement process by increasing the activity of expansin genes and water uptake of the cell in parallel (Gallei et al. 2020; Leyser 2018; Šípošová et al. 2023). Many previous studies in rice showed its role in enhancing coleoptile length and seedling growth during the germination process under dark submergence of rice (Lee et al. 2023; Lu et al. 2023; Nghi et al. 2021; Wu and Yang 2020). Lee et al. (2023) found that there is a threshold level of endogenous IAA for stimulating coleoptile length and repressing root growth. In another study of Nghi et al. (2021), they reported that direct addition of IAA (10 µM) at day 3 of submergence increased the final coleoptile length of only long-coleoptile japonica rice accessions. In our study, we conducted the IAA experiments at different concentrations; the data indicated that the final coleoptile length of all indica rice varieties was improved by the 10 µM IAA treatment. The effect was also displayed at 1 µM of IAA concentration, but it is not clear. In general, these results suggest that the exogenous IAA concentration at 10 µM had a positive influence on the ability of anaerobic germination tolerance in both long and short coleoptile-harboring indica rice accessions. The increase of coleoptile length growth is one of the major factors which decide the anaerobic germination tolerance under flood stress conditions. However, the crucial role of external IAA in the stimulation of coleoptile elongation of indica rice varieties is unclear.

In this study, all rice varieties we used for different experiments belong to indica rice subspecies. They are rice cultivars which are widely cultivated in the Mekong delta area of Vietnam. Analyzing the results obtained from experiments indicated that this indica rice collection had the same ability as the japonica rice in developing long coleoptiles under dark flooded water condition in previous studies. Among them, OM108, OM5451, ĐT8 indica rice varieties showed the great ability of anaerobic germination tolerance. These three rice cultivars developed very long coleoptiles under submergence at both SUB 4D and SUB 8D. The growth curve of coleoptiles of this rice panel from day 0 to day 8 of submergence is also the same to japonica rice subspecies which had studied before. The coleoptile elongation ability of each indica rice cultivar decides their final coleoptile length. We had also demonstrated that IAA concentration at 10 µM displayed clearly the effect on the elongation ability of coleoptiles in both long and short coleoptile-harboring indica rice accessions. These results suggest that OM108, OM5451 and ĐT8 are promising rice cultivars for rice production in the Mekong delta region where using direct seeding methods become more and more popular as well as having to face the risk of flooding yearly. There is a relation between exogenous IAA concentration and the final coleoptile length of our indica rice accession from this study, but its mechanism is still under debate and need further investigations to make it clear.

The study was funded by Tra Vinh University. The authors would like to say thanks to Cuu Long Delta Rice Research Institute for providing rice indica seeds and to colleagues from Application Biology Center of School of Agriculture and Aquaculture, Tra Vinh University for supporting us during the time we conducted the study.

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Article

Research Article

J Plant Biotechnol 2024; 51(1): 63-70

Published online March 28, 2024 https://doi.org/10.5010/JPB.2024.51.007.063

Copyright © The Korean Society of Plant Biotechnology.

Effects of flooding conditions and phytohormones on coleoptile elongation in Indica rice varieties

Khac Nhu Nghi ・Ngoc Ai Trinh

The Institute of Biotechnology, Tra Vinh University, Tra Vinh 87000, Vietnam

Correspondence to:e-mail: nknhu@tvu.edu.vn

Received: 9 March 2024; Revised: 20 March 2024; Accepted: 20 March 2024; Published: 28 March 2024.

This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

The unpredictable scenarios of current climate change pose great challenges for global food security. Climate change triggers submergence, a natural disaster that affects cereal production in the Mekong Delta of Vietnam. Among cereals, rice is a unique species in its ability to germinate and develop a long coleoptile under water. Several previous studies indicated that the capacity of japonica rice is better than indica rice cultivars. Herein, we assessed the ability of coleoptile elongation and the role of exogenous auxin (IAA) in promoting rice coleoptile length under dark, flooded conditions using 20 indica rice varieties collected from the Mekong Delta. We germinated 20 rice seeds per variety under water (with and without adding auxin at different concentrations) for several days and measured the coleoptile length at two different timepoints of submergence. We found that the ability to develop a long coleoptile under water was not related to the rice subspecies. The average coleoptile length at day 8 and the growth curve from the beginning to day 8 of the submergence experiment of our rice cultivars were the same. We also found that 10 μM of IAA concentration expressed a significant effect on the capacity of coleoptile elongation in both long and short coleoptile-harboring indica rice subspecies. Our results suggested that OM108, OM5451, and ĐT8 are promising rice cultivars for rice production in the Mekong Delta of Vietnam.

Keywords: submergence, rice (Oryza sativa L.), auxin, climate change, rice coleoptile

Introduction

Climate change is a negative shift in global climate patterns. It resulted in global warming as well as the increase of extreme weather-related events such as flooding, drought, salinity; wildfire and much more (Arora 2019; Nielsen-Gammon et al. 2020; Seppelt et al. 2022). They impacted directly or indirectly to the livelihood of billions of people over the world, of which there are million global farmers (Arivelarasan et al. 2023; FAO, IFAD, UNICEF, WFP, WHO 2020; Raj et al. 2022). Flooding is one of the most significant challenges for crop production. In a period of 10 years (from 2006 to 2016), it was the reason for almost 70% yield loss of different crops on a global scale (FAO 2018; Patel et al. 2014). Recent studies indicate that there is more than 17 million km2 of global agricultural land affected and billions US dollars lost due to flooded water yearly (Kaur et al. 2020; Vaidya et al. 2024; Voesenek and Sasidharan 2013). The flood predicted areas of agricultural land could grow rapidly in the end of this century, especially in Southeast Asia and India (Coumou and Rahmstorf 2012; Lan et al. 2024).

Currently, feeding more than 8 billion people on the planet is a big challenge for global food production although more than food has been produced during the last decades (Fróna et al. 2019; Strzyżyńska 2022). Among the cereal crops, rice plays an extremely important role in ensuring food security. It is the third leading crop in harvested area and production as well (FAO 2022). Rice is a crucial food supply for more than half of the global population with over 90% of rice cultivated and consumed in Asian countries (Bao 2023; Fukagawa and Ziska 2019; Yu et al. 2021).

Rice is the unique cereal which can germinate in both flooded and anoxic environments (Wu and Yang 2020). Rice is special in ability to create and elongate the coleoptile beyond the water surface in submergence condition in a few days (Miro and Ismail 2013; Yu et al. 2021). However,

rice production is affected seriously by flooding because about one-third of areas used for rice cultivation is usually low and has an annual submerged tendency (Muthayya et al. 2014; Su and Kuo 2023). Millions of hectares of rice-cultivated area were affected with millions of tons of rice lost yearly in the Asia region due to flooding (GriSP 2013; Su and Kuo 2023).

The anaerobic germination tolerance of rice was presented at elongation ability of coleoptiles under flooded water. This ability of rice cultivars is regulated by both division and elongation capacity of cells, with the latter being the major in rice as well as other monocot (Zhang et al. 2021). Cell division plays an important role at the first phase of anaerobic germination, then cell elongation occurs and goes on until the tip of the coleoptile reaches the surface of flooded water.

The certain role of phytohormone in plant response to abiotic stresses such as drought, saltwater intrusion, flooding was well-known (Khan et al. 2012; Zheng et al. 2023). Beside ethylene and gibberellin, auxin (IAA) is the most plentiful hormone which contributed to the growth and development of plant (Gallei et al. 2020; Sosnowski et al. 2023; Vanneste and Friml 2009). Many studies have indicated that IAA plays a key role in improving the germination ability as well as seedling establishment of rice seed under water by stimulating the coleoptile elongation (Lee et al. 2023; Lu et al. 2023; Nghi et al. 2021; Wu and Yang 2020). Nghi et al. (2021) approved that adding directly IAA (10 µM) into the experimental water under dark submergence increased the coleoptile length of japonica rice varieties; whereas, the experimental results of Lee et al. (2023) suggested the high concentration of endogenous auxin enhanced the elongation of coleoptile and repressed the growth of root and the appearance of the first leaf of japonica rice during germination under completely dark submergence. Accumulation of IAA stimulated the coleoptile elongation of japonica rice and the scale is dependent on the rice genotypes (Lee et al. 2023; Nghi et al. 2021; Wu and Yang 2020). Over 500 thousand rice accessions are collected in the global gene bank (Vieira et al. 2022); and although many researches to identify the role of auxin in regulating ability of anaerobic germination tolerance of rice varieties were conducted, the results are still under debate.

In our present study, we assess the ability of coleoptile elongation as well as the role of exogenous IAA in promoting the coleoptile length of indica rice cultivars under dark flooded conditions. These varieties are commonly cultivated rice cultivars in the Mekong delta region of Vietnam. The results indicate that the difference in exogenous auxin concentration and rice genotype determine the final length of both short and long-coleoptile indica rice varieties.

Materials and Methods

Plant material

All 20 rice cultivars used in this study belonged to indica rice subgroup of Oryza sativa L. They were obtained from Cuu Long delta rice research institute and other areas of Mekong rice production region. They widely adapted to the local soil and climatic conditions. Most of them are OM rice accessions which are being popular planted in the fields at Mekong delta. The collected rice seeds were stored in a cold room at 4°C to use for the long term.

Seed germination under dark submergence

The phenotyping experiment was conducted as previously described (Nghi et al. 2019). The rice seed coat was removed and sterilized the surface with 70% ethanol and 3% sodium hypochlorite for 1 min and 15 min; respectively. Then, sterile water was used for washing 3 times after treating ethanol and 5 times after treating sodium hypochlorite. The intact sterile seeds were put on the bottom of magenta boxes where they were covered with a thin layer of sterile cotton. This box was filled with sterile water. The seeds were allowed to germinate at 30°C in the dark submerged condition for 4 and 8 days. 20 seeds of each rice variety were utilized per each experiment and all experiments were repeated 2 times. The coleoptile length at two different time points, then, would be measured using electron digital calipers. The coleoptile samples of rice varieties would be collected and stored to use for subsequent studies.

Auxin experiment

Six rice varieties which were representative of shortest (JASMINE 85, OM4900, OM6976) and longest (ĐT8, OM5451, OM108) coleoptile group at day 8 of submergence (SUB 8D) were selected for the treatments. The rice seeds were treated as described in the above experiments. Each experiment was performed using 20 rice grains. Rice germination occurred in the completely dark submergence and IAA was supplemented directly inside the water environment at day 2 of submergence. The added amount of IAA was calculated in order to ensure the final concentration of the treated environment were 1 µM and 10 µM. At day 8 of submergence, the coleoptile length of the controls and treatments (1 µM and 10 µM) was assessed using electron digital calipers.

Data analysis

We analyzed all data obtained from experiments using statistical program R and Excel software.

Results

The greatly variation in coleoptile elongation ability of indica rice cultivars under submergence

In this experiment, the anaerobic germination ability of 20 indica rice accessions was analyzed through measuring their coleoptile length in different time points (4 days (SUB 4D) and 8 days (SUB 8D) after submergence) under absolutely dark and submergence condition (Fig. 1A). We identified a significant difference in coleoptile length in both SUB 4D and SUB 8D among rice cultivars (Fig. 1A and Table 1). The coleoptile length of rice cultivars of SUB 4D is ranged from 0.95 to 3.11 cm, with a mean value of 1.87 cm; while these data of SUB 8D is from 2.88 to 6.94 cm, with a mean value of 5.11cm (Fig. 1A and Table 1). The CV value of SUB 4D and SUB 8D was 0.35 and 0.21, respectively, indicating that the variation of coleoptile length of SUB 4D was larger (Table 1).

Figure 1. (A) Coleoptile length at days 4 and 8 of submergence of 20 indica rice varieties. (B) Box plot of coleoptile length at days 4 and 8 of submergence among the OM rice group and other rice groups. Values represent the mean ± SD. Student’s t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001

Table 1 . Statistical analysis of traits related to coleoptile length in rice varieties.

TraitMeanSDSERangeCV
Average at Day 4 (mm)18.76.51.59.5–31.10.35
Average at Day 8 (mm)51.110.52.328.8–69.40.21
75th percentile at Day 8 (mm)54.210.72.432.1–74.70.2
Ratio Day 8/43.01.10.21.4–5.70.4


The coleoptile elongation tendency under flooded water of these indica rice cultivars is unstable in 2 different time points under complete dark submergence. While variety CL309 and OM 6976 always belong to longest and shortest coleoptile groups, respectively, at both day 4 and day 8 after submergence; ST23 and OM576 rice cultivars indicated the contrary trend in 2 different time points. ST23 is located in the longest group at day 4 and shortest group at day 8, whereas the variety OM576 is vice versa. The coleoptile of OM5451 and OM108 is medial at first 4 days of submergence, but their coleoptile elongation ability was strong and displayed very long coleoptile after next 4 days of submergence (Fig. 1A).

The difference in coleoptile length between OM rice group and the other on 4th day of submergence

An analysis of the difference in coleoptile length among rice accessions at day 4 and day 8 of submergence was conducted. We divided these rice varieties into two groups (OM group and other) and analyzed the coleoptile length variation between them at 2 time points of experiment. The results indicated that the coleoptile which was developed from accessions of OM group of SUB 4D is significantly shorter than the other, whereas there is no significant difference in coleoptile length observed between two groups of SUB 8D (Fig. 1B). In our results, the rice varieties OM108 and OM576 (belonged to OM group) showed the longest coleoptile lengths at SUB 8D (Fig. 1A).

The coleoptile growth speed of the collected indica rice accessions

We selected two subgroup of rice varieties (three varieties per each), which developed the longest and shortest coleoptile in length at SUB 8D, to identify the developmental tendency and the growth rate (displayed by the trait ratio 8D/4D) of their coleoptile from day 1 to day 8 under dark submergence (Fig. 2A, E). The analyzed result indicated that the elongation speed is different between not only selected rice of 2 subgroups but also in whole our indica rice accessions (Fig. 2B). The growth curve of these selected subgroups showed the rate of coleoptile elongation is relatively slow from day 0 to 4 of submergence; reach an exponential growth between 4 and 6 days; slow down and go to the plateau stage from day 7 to 8 of submergence (Fig. 2C, D).

Figure 2. (A) The average length of long (OM108, OM5451, and ĐT8) and short coleoptile (JASMINE85, OM6976, and OM4900) rice variety groups at days 4 and 8 of submergence (mean ± SD). Student's t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001. (B) The ratio between SUB 8D and SUB 4D of coleoptile length of indica rice accessions. (C and D) Growth curve of coleoptile length from days 0-8 of long and short coleoptile rice variety groups under dark submergence (mean ± SD). Student’s t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001. (E) Coleoptile length SUB 8D of six chosen rice varieties.

The effect of IAA (auxin) on elongation of rice coleoptile under submergence

In order to understand the IAA role in determining the final length of rice coleoptile after 8 days of germination under submergence, we conducted other experiments using the same of two above subgroups of rice varieties. IAA was utilized in the experiments with two different concentrations (1 µM and 10 µM). We found that IAA addition in experimental water impacted the coleoptile elongation ability of rice cultivar. The scale depends on IAA concentration and kind of rice accession (Fig. 3).

Figure 3. (A) Influence of IAA (1 µM) treatment at day 2 on the final coleoptile length of long and short coleoptile rice variety groups under dark submergence (mean ± SD). (B) Influence of IAA (10 µM) treatment at day 2 on the final coleoptile length of long and short coleoptile rice variety groups under dark submergence (mean ± SD). (C) Coleoptile length between control and treatment of JASMINE85 and ĐT8 rice varieties. Values represent the mean ± SD. Student’s t-test: Not statistically (ns) significant (P > 0.05); statistically significant (P ≤ 0.05). Lowercase letters indicate significant differences among treatments.

In the first IAA experiment, we tried with 1 µM of IAA. The result indicated that, in general, there is a significant variation in coleoptile length between the control and treatment of two subgroups at SUB 8D. But If we go in detail, only the OM4900 (representative of the shortest group) and OM108 (representative of the longest group) displayed the great difference (Fig. 3A). Whereas, adding IAA at 10 µM of concentration showed a positive influence on the final length of coleoptile in whole rice varieties used in the experiment (Fig. 3B, C). The coleoptile length of the treatment is much longer than the control one at SUB 8D (Fig. 3B, C).

Discussion

Because of the shortage of fresh water and labor resources as well as the increase of input cost, direct seeding became a major method for rice production (Aung et al. 2023; Miro and Ismail 2013) and the ability of rice cultivars to develop a long coleoptile under flooded water is significant. Many previous studies indicated that this ability of japonica rice varieties was better than indica one (Aung et al. 2023; Nghi et al. 2019; Su et al. 2021; Zhang et al. 2017). However, our results showed a high coleoptile elongation capacity of indica accession. Our indica group could develop a long coleoptile with the average length was even the same to japonica group of Nghi et al. (2019) at Day 8 of dark submergence at 30°C (5.11 cm in comparison with 5.15 cm) (Table 1).

Mekong delta is the biggest region for rice production in Vietnam. It makes up over 50% of harvested area and 60% of rice productivity of Vietnam (Vietnam general statistics office 2021). Among rice cultivars which are generally cultivating in this delta, OM rice varieties are in the majority. These rice cultivars were developed from Cuu Long delta rice research institute of Vietnam. Therefore, we decided to divide our indica rice accessions into two group are OM group and other group. In our studies, the rice varieties OM108 and OM576 which showed the longest coleoptile lengths SUB 8D belonged to OM group (Fig. 1a). OM rice varieties are commonly cultivated rice varieties at Mekong delta region of Vietnam because they were bred over several generations to widely adapt to cultivation strategy of direct seeding and different agroecosystems in this area (Le and Umetsu 2022). Therefore, the ability of developing a long coleoptile under submergence is a crucial property.

The difference of coleoptile length between 2 time points of submergence of each rice variety in our indica rice panel was significant. Some varieties such as OM576, OM5451 developed coleoptiles to be among shortest and medium groups at SUB 4D; whereas at SUB 8D their coleoptile length belonged to the longest one (Fig. 1A). There are several factors affecting this property. Many previous studies revealed that several genes in rice related to extension of anaerobic germination ability show a significantly different expression level in different time points of germination stage of rice seed (He et al. 2023; Magneschi et al. 2009; Nghi et al. 2019; Su et al. 2021; Zhang et al. 2017).

The coleoptile length of each rice variety depends on their elongation rate under water. In our study, the selected rice varieties between two subgroups created coleoptiles with significant difference in length at SUB 8D. Analyzing the growth model of coleoptile between our two subgroups indicated that the difference in coleoptile length from the beginning to day 3th of germination is not really great; the elongation rate began to become significantly different from day 4th and reach greatest and stable at day 7th and later of germination (Fig. 2C, D). Several previous researches in japonica rice also displayed the same pattern as our study (He et al. 2023; Magneschi et al. 2009; Nghi et al. 2019). It suggests that the coleoptile growth pattern is the same for both indica and japonica rice cultivars which showed the ability of anaerobic germination tolerance. The variation in coleoptile elongation rate decided their final length.

Auxin (IAA) is a phytohormone which has the crucial role in promoting the growth of tip parts of the plant through stimulating cell wall enlargement process by increasing the activity of expansin genes and water uptake of the cell in parallel (Gallei et al. 2020; Leyser 2018; Šípošová et al. 2023). Many previous studies in rice showed its role in enhancing coleoptile length and seedling growth during the germination process under dark submergence of rice (Lee et al. 2023; Lu et al. 2023; Nghi et al. 2021; Wu and Yang 2020). Lee et al. (2023) found that there is a threshold level of endogenous IAA for stimulating coleoptile length and repressing root growth. In another study of Nghi et al. (2021), they reported that direct addition of IAA (10 µM) at day 3 of submergence increased the final coleoptile length of only long-coleoptile japonica rice accessions. In our study, we conducted the IAA experiments at different concentrations; the data indicated that the final coleoptile length of all indica rice varieties was improved by the 10 µM IAA treatment. The effect was also displayed at 1 µM of IAA concentration, but it is not clear. In general, these results suggest that the exogenous IAA concentration at 10 µM had a positive influence on the ability of anaerobic germination tolerance in both long and short coleoptile-harboring indica rice accessions. The increase of coleoptile length growth is one of the major factors which decide the anaerobic germination tolerance under flood stress conditions. However, the crucial role of external IAA in the stimulation of coleoptile elongation of indica rice varieties is unclear.

Conclusion

In this study, all rice varieties we used for different experiments belong to indica rice subspecies. They are rice cultivars which are widely cultivated in the Mekong delta area of Vietnam. Analyzing the results obtained from experiments indicated that this indica rice collection had the same ability as the japonica rice in developing long coleoptiles under dark flooded water condition in previous studies. Among them, OM108, OM5451, ĐT8 indica rice varieties showed the great ability of anaerobic germination tolerance. These three rice cultivars developed very long coleoptiles under submergence at both SUB 4D and SUB 8D. The growth curve of coleoptiles of this rice panel from day 0 to day 8 of submergence is also the same to japonica rice subspecies which had studied before. The coleoptile elongation ability of each indica rice cultivar decides their final coleoptile length. We had also demonstrated that IAA concentration at 10 µM displayed clearly the effect on the elongation ability of coleoptiles in both long and short coleoptile-harboring indica rice accessions. These results suggest that OM108, OM5451 and ĐT8 are promising rice cultivars for rice production in the Mekong delta region where using direct seeding methods become more and more popular as well as having to face the risk of flooding yearly. There is a relation between exogenous IAA concentration and the final coleoptile length of our indica rice accession from this study, but its mechanism is still under debate and need further investigations to make it clear.

Acknowledgement

The study was funded by Tra Vinh University. The authors would like to say thanks to Cuu Long Delta Rice Research Institute for providing rice indica seeds and to colleagues from Application Biology Center of School of Agriculture and Aquaculture, Tra Vinh University for supporting us during the time we conducted the study.

Fig 1.

Figure 1.(A) Coleoptile length at days 4 and 8 of submergence of 20 indica rice varieties. (B) Box plot of coleoptile length at days 4 and 8 of submergence among the OM rice group and other rice groups. Values represent the mean ± SD. Student’s t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001
Journal of Plant Biotechnology 2024; 51: 63-70https://doi.org/10.5010/JPB.2024.51.007.063

Fig 2.

Figure 2.(A) The average length of long (OM108, OM5451, and ĐT8) and short coleoptile (JASMINE85, OM6976, and OM4900) rice variety groups at days 4 and 8 of submergence (mean ± SD). Student's t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001. (B) The ratio between SUB 8D and SUB 4D of coleoptile length of indica rice accessions. (C and D) Growth curve of coleoptile length from days 0-8 of long and short coleoptile rice variety groups under dark submergence (mean ± SD). Student’s t-test, nsP > 0.05, *P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001. (E) Coleoptile length SUB 8D of six chosen rice varieties.
Journal of Plant Biotechnology 2024; 51: 63-70https://doi.org/10.5010/JPB.2024.51.007.063

Fig 3.

Figure 3.(A) Influence of IAA (1 µM) treatment at day 2 on the final coleoptile length of long and short coleoptile rice variety groups under dark submergence (mean ± SD). (B) Influence of IAA (10 µM) treatment at day 2 on the final coleoptile length of long and short coleoptile rice variety groups under dark submergence (mean ± SD). (C) Coleoptile length between control and treatment of JASMINE85 and ĐT8 rice varieties. Values represent the mean ± SD. Student’s t-test: Not statistically (ns) significant (P > 0.05); statistically significant (P ≤ 0.05). Lowercase letters indicate significant differences among treatments.
Journal of Plant Biotechnology 2024; 51: 63-70https://doi.org/10.5010/JPB.2024.51.007.063

Table 1 . Statistical analysis of traits related to coleoptile length in rice varieties.

TraitMeanSDSERangeCV
Average at Day 4 (mm)18.76.51.59.5–31.10.35
Average at Day 8 (mm)51.110.52.328.8–69.40.21
75th percentile at Day 8 (mm)54.210.72.432.1–74.70.2
Ratio Day 8/43.01.10.21.4–5.70.4

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Vol 51. 2024

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