Adaptive Diversity of Echinochloa Species to Osmotic Stress
  • Adaptive Diversity of Echinochloa Species to Osmotic Stress
  • Seon-Ju Park , Hye-Jin Yu , Min-Jung Yook , Do-Soon Kim
  • Weed & Turfgrass Science.2016. Dec, 5(4): 181-186
    DOI : http://dx.doi.org/10.5660/WTS.2016.5.4.181

  • Weed&Turfgrass Science was renamed from both formerly Korean Journal of Weed Science from Volume 32 (3), 2012, and formerly Korean Journal of Turgrass from Volume 25 (1), 2011 and Asian Journal of Turgrass Science from Volume 26 (2), 2012 which were launched by The Korean Society of Weed Science and the Turfgrass Society of Korea founded in 1981 and 1987, respectively.
  • Copyright @ 2016, The Korean Society of Weed Science and The Turfgrass Society of Korea Archive
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Abstract
Three Echinochloa species inhabit various crop fields with different soil moisture conditions. Therefore, a growth pouch test was conducted to investigate adaptive diversity of six Echinochloa species, three from Korea and three from USA, to osmotic stress by assessing shoot and root growths. Echinochloa crus-galli var. praticola showed the greatest tolerance to osmotic stress in both root (GR 50 =1316.3 g PEG L -1 ) and shoot (GR 50 =212.2 g PEG L -1 ) growths, while Korean E. oryzicola was most sensitive to osmotic stress in both root (GR 50 =116 g PEG L -1 ) and shoot (GR 50 =126.2 g PEG L -1 ) growths. Root to shoot (R/S) ratio of Echinochloa crus-galli var. praticola increased with increasing osmotic stress, while that of Korean E. oryzicola decreased, suggesting that R/S ratio is closely related to osmotic stress tolerance in Echinochloa species. Our results clearly demonstrate that E. crus-galli var. praticola maintains high R/S ratio even under high osmotic stress, which enables this species to well adapt to dry upland condition. In contrast, while E. oryzicola fails to maintain sufficiently high R/S ratio, resulting in poor adaptability to dry upland condition.
Keywords
Introduction
Echinochloa genus is composed of around 50 species, which are distributed around the world ( Holm et al. 1977 ). Although some of Echinochloa species used to be cultivated as a food crop, most of them are now regarded as problematic weeds because of their high competitiveness against crop under various environmental conditions, causing inevitable crop yield losses (e.g. Moon et al., 2010 and 2014 ). Several studies related with environmental stresses such as flooding ( Kim, 1993 ; Im, 2016 ), salt ( Aslam et al., 1987 ; Yamamoto et al., 2003 ; Kim et al., 2004 ; Nguyen et al., 2005 ), and drought ( Hamin et al., 2016 ) were supporting that Echinochloa species have higher tolerance than cultivated rice and so on. Regarding drought stress, Hamim et al. (2016) performed seedling experiment and discovered physiological and anatomical changes of E. crus-galli during drought stress and recovering. However, drought stress-related experiments with Echinochloa were very limited so far because controlling soil moisture is uneasy. Two Echinochloa species are known to be naturally distributed in Korea such as E. oryzicola Vasing and E. crus-galli (L.) Beauv. Echinochloa crus-galli is then subdivided into two varieties such as E. crus-galli var. crus-galli and E. crus-galli var. praticola depending on their morphological traits and habitats. Echinochoa oryzicola inhabits only flooded rice paddy field, while E. crus-galli inhabits various field conditions from paddy field to dry upland ( Yamasue et al. 1989 ). In E. crus-galli , E. crus-galli var. praticola inhabits upland field only, while E. crus-galli var. crus-galli inhabits areas from dry land to paddy field. These various habitats of three Echinochloa species imply that adaptive diversity to abiotic stress exists in Echinochloa species.
The three Echinochloa species inhabiting Korea have close morphological similarity except for several traits particularly those related to seed such as seed awn and seed size. In ploidy level, E. oryzicola is tetraploid (2n = 4X =36), while E. crus-galli is hexaploid (2n = 6X = 54) revealed by flow cytometric analysis and chromosome counting ( Nah et al., 2015a ). It is known that Echinochloa crus-galli is an allohexaploid produced by natural hybridization between tetraploid E. oryzicola and unknown diploid Echinochloa species and then subsequent chromosome doubling ( Yabuno, 1966 ). Echinochloa crus-galli was then further developed into new biological sub-species with various water-condition adaptabilities. Therefore, it can be hypothesized that Echinochloa species have expanded their habitats from flooded condition to dry upland condition during evolution processes including natural hybridization and chromosome doubling, enabling Echinochloa crus-galli to have more diverse environmental adaptability than E. oryzicola . Eco-physiologically Korean Echinochloa species, E. oryzicola , E. crus-galli var. crus-galli , and E. crus-galli var. praticola , have their favorite habitats depending on soil water conditions. Seed germination study showed that under deep water flooding condition, E. oryzicola could germinate better than E. crus-galli ( Kim, 1993 ), suggesting that adaptive diversity to flooding condition exists in Echinochloa species and E. oryzicola better adapts to flooded condition than E. crus-galli . However, it is unclear how Echinochloa species respond to osmotic stress. No studies have been conducted about the diverse response and adaptability of Echinochloa spp. to dry soil condition.
Therefore, this study was conducted to investigate the growth response and adaptability of Echinochloa spp. to dry soil condition by using growth pouch method ( Zhang et al., 2015 ). Dry soil condition was artificially provided using polyethylene glycol (PEG), which has often been used to give different levels of osmotic stress (e.g., O'Donnell et al., 2013 ).
Materials & Methods
- Plant materials
Six Echinochloa species were used in this experiment. Three of them were collected in Korea such as Echinochloa crus-galli var. praticola (ECHPT-KO), E. crus-galli (ECHCG-KO), and E. oryzicola (ECHOR-KO), and the other three species were collected in California, USA such as E. crus-galli (ECHCG-US), E. oryzoides (ECHOZ-US), and E. oryzicola (ECHOR-US).
- Growth pouch test under osmotic stress
Seeds of Echinochloa species were incubated in petri dishes in a plant growth chamber maintained at 30/20 ℃ of temperature (day/night). When seeds were germinated, the germinated seeds were transplanted into 7-mL PEG-containing (without nutrient solution) growth pouches and incubated in the plant growth chamber with 16 hours of photoperiod. Dark condition was maintained for the roots by placing the growth pouches in a top-open paper box. The schematic illustration of the growth pouch method is shown in Fig. 1 . The PEG-6000 was used to mimic dry soil conditions and a range of PEG concentrations were given; 0 g, 40 g, 80 g, 120 g, and 160 g PEG L -1 . Deionized water was added to the growth pouches every day to compensate for evaporation. At 6 days after PEG treatment (DAT), root and shoot lengths were measured. The experiment consisted of four replicates of a split-split plot design with 5 concentrations of PEG as the main plot, which was then split with 6 Echinochloa species as subplots.
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Schematic illustration of the growth pouch test with PEG solution.
- Statistical analysis
All measurements were initially subjected to analysis of variance (ANOVA). Non-linear regression analysis was conducted by fitting the log-logistic model ( Streibig, 1980 ) to the root and shoot lengths observed at 6 days after sowing. All statistical analyses were conducted using Genstat ( Genstat Committee, 2002 ).
Results and Discussion
- Root growth response ofEchinochloaspecies to osmotic stress
To clearly investigate root growth response of Echinochloa to osmotic stress by avoiding the effects on seed germination, pre-germinated seeds were exposed to PEG solutions at a range of PEG concentrations. All tested Echinochloa species showed various responses to PEG in their root growths up to 6 DAT ( Fig. 2 ). Among them, Echinochloa crus-galli var. praticola (ECHPT-KO) was the least influenced by PEG treatment in its root growth, while the other five Echinochloa species showed significant decreases in their root growths ( Fig. 2 ). At no PEG treatment, two Korean Echinochoa crus-galli species (ECHCG-KO and ECHPT-KO) showed the smallest roots with 4.52 cm and 4.94 cm of root lengths at 6 DAT, respectively, while Korean E. oryzicola (ECHOR-KO) showed the longest root, 9.70 cm, followed by E. oryzoides (ECHOZ-US), E. crus-galli (ECHCG-US), and E. oryzicola (ECHOR-US) from the USA with root lengths of 8.12 cm, 7.01 cm, and 6.58 cm, respectively. With increasing PEG concentration, the root growth of Echinochloa species was significantly affected except for ECHPT-KO. ANOVA revealed that osmotic stress by PEG significantly inhibited root growths of 2 Korean Echinochloa species, ECHCG-KO and ECHOR-KO, and 3 American Echinochloa species, ECHCG-US, ECHOZ-US, and ECHOR-US, while osmotic stress did not significantly inhibit the root growth of ECHPT-KO ( Table 1 ). This result suggests that Echinochloa crus-galli var. praticola is much more tolerant to osmotic stress in its root growth than the other tested Echinochloa species.
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Root lengths of 3 Korean Echinochloa species (E. crus-galli var. praticola (ECHPT-KO), E. crus-galli var. crus-galli (ECHCGKO), and E. oryzicola (ECHOR-KO)) and 3 American Echinochloa species (E. crus-galli (ECHCG-US), E. oryzoides (ECHOZ-US), and E. oryzicola (ECHOR-US)) grown in the growth pouch containing a range of PEG concentrations.
Summary of analysis of variance (ANOVA)
Echinochloa spp. Root length Shoot length R/S ratio
ECHPT-KO 1.59NS 8.16** 2.66NS
ECHCG-KO 5.23** 9.09** 1.27NS
ECHOR-KO 28.17*** 60.87*** 5.51**
ECHCG-US 43.58*** 9.16*** 15.55***
ECHOZ-US 12.29*** 12.71** 0.69NS
ECHOR-US 13.7*** 16.59*** 2.90NS
NSindicates no significance at P=0.05
**and ***indicate significance at P=0.01 and P= 0.001, respectively
Non-linear regression by fitting the log-logistic model to the root lengths at a range of PEG concentrations at 6 DAT could estimate the maximum root growth at no PEG treatment and the GR 50 values, the PEG concentrations required for 50% root growth inhibition for each Echinochloa species ( Table 2 and Fig. 3 ). The GR 50 value for root length at 6 DAT was the least in ECHOR-KO with 116 g PEG L -1 , followed by ECHCG-US, ECHOZ-US, ECHOR-US, and ECHCG-KO with 130.3 g, 144.8 g, 153.2 g, and 156.1 g PEG L -1 , respectively. Exceptionally ECHPT-KO showed extremely high GR 50 value with over 1300 g PEG L -1 , almost 10 times greater than those of the other Echinochloa species. However, the estimation for ECHPT-KO was not accurate due to lack of observed values at higher concentrations than 160 g PEG L -1 , so an additional test with high concentrations of PEG is required in order to estimate more accurate GR 50 value. Nonetheless, our results clearly indicate that E. crus-galli var. praticola (ECHPT-KO) is the most tolerant to osmotic stress, while E. oryzicola (ECHOR-KO) is the most sensitive to osmotic stress in root growth response.
Parameter estimates for the log-logistic model fitted to root lengths ofEchinochloaspecies grown under a range of PEG concentration. The numbers in parentheses are the standard errors.
Echinochloa spp. Parameter estimates R2
Y0 GR50 B
ECHPT-KO 4.88 (NA) 1316.3 (NA) 1.53 (0.89) 0.015
ECHCG-KO 4.92 (0.379) 156.1 (21.07) 2.42 (1.14) 0.577
ECHOR-KO 9.09 (0.521) 116.0 (7.31) 4.81 (1.34) 0.843
ECHCG-US 7.91 (0.358) 130.3 (6.12) 5.21 (1.33) 0.840
ECHOZ-US 8.53 (0.558) 144.8 (16.51) 2.14 (0.74) 0.698
ECHOR-US 6.85 (0.390) 153.2 (12.56) 3.31 (1.24) 0.678
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Responses of 3 Korean Echinochloa species (E. crus-galli var. praticola (a), E. crus-galli var. crus-galli (b), and E. oryzicola (c)) and 3 American Echinochloa species (E. crus-galli (d), E. oryzoides (e), and E. oryzicola (f)) in their root growths to PEG solution. Root lengths were measured at 6 days after placing germinated seeds on the paper wick of the growth pouch.
- Shoot growth response ofEchinochloaspecies to osmotic stress
After placing germinated seeds of Echinochloa species, shoot growth was also daily recorded up to 6 DAT ( Fig. 4 ). All Echinochloa species significantly responded to increasing PEG concentrations with no exception. At no PEG treatment, E. crus-galli var. praticola (ECHPT-KO) was the smallest with 3.72 cm plant height, while American E. oryzicola (ECHOR-US) was the tallest with 9.38 cm plant height. The other species were around 5-6 cm tall. At PEG treatment, Korean E. oryzicola (ECHOR-KO) was most significantly affected in its shoot growth by PEG, while E. crus-galli var. praticola (ECHPT-KO) was least significantly affected by PEG ( Fig. 4 and Table 1 ). At 120 g PEG L -1 , ECHPT-KO showed the least growth reduction of 24%, followed by ECHCG-US, ECHOZ-US, ECHOR-KO, ECHCG-KO, and ECHOR-US with 31%, 37%, 40%, 46%, and 51% growth reduction, respectively ( Fig. 4 ). At 160 g PEG L -1 , ECHPT-KO still maintained good shoot growth, while ECHOR-KO showed significant growth inhibition, resulting in the greatest shoot growth reduction of 84%. In overall, our results indicate that E. crus-galli var. praticola is the most tolerant to osmotic stress in shoot growth, while E. oryzicola is the most sensitive to osmotic stress.
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Shoot lengths of 3 Korean Echinochloa species (E. crus-galli var. praticola (ECHPT-KO), E. crus-galli var. crus-galli (ECHCGKO), and E. oryzicola (ECHOR-KO)) and 3 American Echinochloa species (E. crus-galli (ECHCG-US), E. oryzoides (ECHOZ-US), and E. oryzicola (ECHOR-US)) grown in the growth pouch containing a range of PEG concentrations.
Non-liner regression analysis revealed that Echinochloa shoot growth responding to PEG concentration is well described by the log-logistic model, resulting in estimation of GR 50 values, the PEG concentration causing 50% shoot growth reduction ( Table 3 and Fig. 5 ). The GR 50 value for shoot length at 6 DAT was the least in ECHOR-KO with 126.2 g PEG L -1 , followed by ECHCG-KO, ECHOR-US, and ECHOZ-US with 128.8 g, 134.6 g, and 168.3 g PEG L -1 , respectively. ECHPT-KO showed the greatest GR 50 value of 212.2 g PEG L -1 , and ECHCG-US also showed a similar GR 50 value of 205.1 g PEG L -1 . Similarly to root growth response, these results also suggest that E. crus-galli var. praticola (ECHPT-KO) is the most tolerant to osmotic stress, while E. oryzicola (ECHOR-KO) is the most sensitive to osmotic stress in shoot growth response. Interestingly American E. oryzicola was much taller than Korean E. oryzicola . This difference may be due to different water management during early growth stage from planting. Korean rice cultivation is mainly by machine-transplanting under flooded paddy condition at around 5 cm water depth, while Californian rice cultivation is mainly by airplane-direct-sowing under deep flooded paddy condition at deeper than 10 cm water depth, suggesting that continuous deep water rice culture in California may have selected submergence tolerant and fast growing E. oryzicola in California.
Parameter estimates for the log-logistic model fitted to shoot lengths ofEchinochloaspecies grown under a range of PEG concentration. The numbers in parentheses are the standard errors.
Echinochloa spp. Parameter estimates R2
Y0 GR50 B
ECHPT-KO 3.80 (0.232) 212.2 (52.20) 1.27 (0.504) 0.630
ECHCG-KO 5.55 (0.413) 128.8 (17.77) 1.85 (0.623) 0.705
ECHOR-KO 6.12 (0.212) 126.2 (3.66) 7.55 (1.70) 0.913
ECHCG-US 4.98 (0.239) 205.1 (33.23) 1.92 (0.722) 0.680
ECHOZ-US 5.42 (0.302) 168.3 (20.70) 1.96 (0.674) 0.705
ECHOR-US 9.50 (0.557) 134.6 (20.99) 1.25 (0.344) 0.766
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Responses of 3 Korean Echinochloa species (E. crus-galli var. praticola (a), E. crus-galli var. crus-galli (b), and E. oryzicola (c)) and 3 American Echinochloa species (E. crus-galli (d), E. oryzoides (e), and E. oryzicola (f)) in their root growths to PEG solution. Shoot lengths were measured at 6 days after placing germinated seeds on the paper wick of the growth pouch.
- Response ofEchinochloaspecies in their R/S ratio to osmotic stress
Plant shoot is a sink of water, while root is a source of water. Under sufficient water supply condition, it is better for plant to maintain low root and shoot (R/S) ratio. However, if water is limited, plant instantly alter its strategy, so minimizing shoot growth to avoid or minimize water loss from leaves but maintaining or promoting root growth to maximize water uptake from soil. Therefore, under osmotic stress, increasing R/S ratio is a common phenomenon often observed in osmotic stress tolerant plant.
At no PEG treatment, wide variation of R/S ratio exists among Echinochloa species. ECHOR-KO showed the greatest R/S ratio of 1.68, followed by ECHOZ-US, ECHCG-US, ECHPT-KO, ECHCG-KO, and ECHOR-US with R/S ratios of 1.57, 1.34, 1.23, 0.88, and 0.70, respectively ( Fig. 6 ). ANOVA showed that PEG treatment significantly affected R/S ratios of ECHOR-KO and ECHCG-US, while no significantly affected those of the other Echinochloa species. The R/S ratio of E. crus-galli var. praticola (ECHPT-KO) was even smaller than that of Korean E. oryzicola (ECHOR-KO). However, with increasing PEG concentration, there is a clear trend of increase in R/S ratio of E. crus-galli var. praticola , while Korean E. oryziola showed opposite trend of decreasing R/S ratio although its R/S ratio was greatest at no PEG treatment ( Fig. 6 ). In the case of American E. oryzicola (ECHOR-US), its R/S ratio was smallest and showed no significant change with increasing PEG concentration. Although it is difficult to explain variation in adaptability of Echinochoa species only using R/S ratio, our finding supports that E. crus-galli var. praticola increases R/S ratio with increasing osmotic stress, while E. oryzicola decreases R/S ratio or shows smallest R/S ratio. This difference in R/S ratio between E. crus-galli var. praticola and E. oryzicola may explain why these two Echinochloa species have contrasting adaptability to osmotic stress by differently responding to osmotic stress in their root and shoot growths.
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Root and shoot (R/S) ratios of 3 Korean Echinochloa species (E. crus-galli var. praticola (ECHPT-KO), E. crus-galli var. crus-galli (ECHCG-KO), and E. oryzicola (ECHOR-KO)) and 3 American Echinochloa species (E. crus-galli (ECHCGUS), E. oryzoides (ECHOZ-US), and E. oryzicola (ECHOR-US)) grown in the growth pouch containing a range of PEG concentrations. Root and shoot ratios were estimated by dividing root lengths by shoot lengths measured at 6 days after placing germinated seeds on the paper wick of the growth pouch.
- Adaptive diversity ofEchinochloaspecies to osmotic stress
It is known that Echinochloa species have diverse ecological adaptability, which was recently investigated in transcriptome level ( Nah et al., 2015a ). Many of these studies have focused on adaptation to flooding stress ( Kim, 1993 ; Im, 2016 ). In the case of osmotic stress, due to difficulty of experiment, many of studies investigated seed germination response to osmotic stress. In our study, the growth pouch method ( Zhang et al., 2015 ) enabled us to investigate root and shoot growth responses to osmotic stress in detail. From the results in this study, shoot and root growth of all the tested Echinochloa species were inhibited with increasing PEG concentration, suggesting that Echinochloa species were negatively affected by drought stress. A previous study tested with seedlings of E. crus-galli under drought stress ( Hamin et al., 2016 ) showed similar response. Meanwhile, salt stress includes both osmotic and ionic stresses and plants respond rapidly to osmotic stress ( Huang et al., 2012 ; Munns and Tester, 2008 ). Therefore, several studies on Echinochloa species in relation to salt stress ( Yamamoto et al., 2003 ; Kim et al., 2004 ; Nguyen et al., 2005 ) support our result. Our findings also demonstrate that E. crus-galli var. praticola (ECHPT-KO) maintains root growth and minimizes shoot growth inhibition by osmotic stress, resulting in increased R/S ratio with increasing PEG concentration. In contrast, E. oryzicola responds to osmotic stress significantly in its root and shoot growth, resulting in decreased R/S ratio of Korean E. oryzicola (ECHOR-KO) and lowest R/S ratio of American E. oryzicola (ECHOR-US). These contrasting responses to osmotic stress explain why E. crus-galli var. praticola inhabits dry upland field and E. oryzicola inhabits only flooded paddy field. The other 3 Echinochloa species, ECHCG-KO, ECHCG-US, and ECHOZ-US, showed intermediate adaptability to osmotic stress. Therefore, our results clearly demonstrate genetic diversity of Echinochloa species in their adaptation to osmotic stress. Simple sequence repeat (SSR) marker analysis clustered Echinochloa species into two groups, E. oryzicola and E. crus-galli ( Lee et al., 2016 ). In E. crus-galli group, their phylogenetic relationships are more complex than those in E. oryzicola , indicating high genetic diversity in E. crus-galli . This is also in agreement with our findings in this study, which revealed more diverse adaptability in E. crus-galli than E. oryzicola . Different responses of Echinochloa species to osmotic stress indicate different tolerances to osmotic stress among Echinochloa species, playing an important role in determining favorite habitats of Echinochloa species. To uncover mechanism of osmotic stress tolerance which determines such an adaptive diversity in Echinochloa species, molecular approaches are required by using genetic information from previous genomic studies ( Nah et al., 2015b ; Yang et al., 2013 ). Our report is the first result to reveal the reason why E. crus-galli var. praticola is predominantly found in dry upland fields, while E. oryzicola is not found in dry upland fields but only in flooded paddy fields. This study can be a basis to explain diverse adaptability of Echinochloa spp. in relation to soil moisture.
Acknowledgements
This work was carried out with the support of the “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01052602)”, Rural Development Administration, Republic of Korea.
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