Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2011 Jan;23(1):412-27.
doi: 10.1105/tpc.110.080325. Epub 2011 Jan 14.

The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice

Takeshi Fukao  1 , Elaine Yeung, Julia Bailey-Serres
Affiliations

The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice

Takeshi Fukao et al. Plant Cell. 2011 Jan.

Abstract

Submergence and drought are major constraints to rice (Oryza sativa) production in rain-fed farmlands, both of which can occur sequentially during a single crop cycle. SUB1A, an ERF transcription factor found in limited rice accessions, dampens ethylene production and gibberellic acid responsiveness during submergence, economizing carbohydrate reserves and significantly prolonging endurance. Here, we evaluated the functional role of SUB1A in acclimation to dehydration. Comparative analysis of genotypes with and without SUB1A revealed that SUB1A enhanced recovery from drought at the vegetative stage through reduction of leaf water loss and lipid peroxidation and increased expression of genes associated with acclimation to dehydration. Overexpression of SUB1A augmented ABA responsiveness, thereby activating stress-inducible gene expression. Paradoxically, vegetative tissue undergoes dehydration upon desubmergence even though the soil contains sufficient water, indicating that leaf desiccation occurs in the natural progression of a flooding event. Desubmergence caused the upregulation of gene transcripts associated with acclimation to dehydration, with higher induction in SUB1A genotypes. SUB1A also restrained accumulation of reactive oxygen species (ROS) in aerial tissue during drought and desubmergence. Consistently, SUB1A increased the abundance of transcripts encoding ROS scavenging enzymes, resulting in enhanced tolerance to oxidative stress. Therefore, in addition to providing robust submergence tolerance, SUB1A improves survival of rapid dehydration following desubmergence and water deficit during drought.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
SUB1A Confers Drought Tolerance to Rice. (A) Photos of rice plants treated with drought. Twenty plants of each M202 and M202(Sub1) line were grown in the same pot for 14 d and subjected to drought treatment for 8 d. After the treatment, plants were recovered under regular watering conditions for 14 d. Bars = 10 cm. (B) Viability of plants after 8 d of drought treatment and 14 d of recovery. Plants were counted as viable when one or more leaves were produced during the recovery period. Data represent mean ± se (n = 20 × 3 independent biological replicates), and an asterisk indicates a significant difference between M202 and M202(Sub1) (P < 0.05). (C) Fresh weight of aerial tissue before and after drought treatment. Data are represented as in (B). (D) RWC of fully expanded uppermost leaf during drought. Data represent mean ± se (n = 8), and an asterisk indicates a significant difference between M202 and M202(Sub1) (*P < 0.05; **P <0.01). (E) Lipid peroxidation in aerial tissue during drought. The level of MDA, an end product of lipid peroxidation, was monitored in aerial tissue of plants treated with water deficit. Data represent mean ± se (n = 3), and an asterisk indicates a significant difference between M202 and M202(Sub1) (P < 0.05). FW, fresh weight. (F) Relative mRNA levels of SUB1 genes in aerial tissue during drought. Fourteen-day-old plants were exposed to water deficit for up to 5 d. Aerial tissue was harvested at the time points specified and analyzed by qRT-PCR. Relative level of each transcript was calculated by comparison to the nonstressed control [M202(Sub1) at day 0 for SUB1A; M202 at day 0 for SUB1B and SUB1C]. Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between M202 and M202(Sub1) (P < 0.01).
Figure 2.
Figure 2.
SUB1A Enhances mRNA Accumulation of Genes Associated with Acclimation to Drought. mRNA levels were measured in leaves of plants subjected to 0, 3, 4, or 5 d of drought and are expressed relative to the level in M202 at day 0 (set at 1.0). Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between M202 and M202(Sub1) (*P < 0.05; **P < 0.01).
Figure 3.
Figure 3.
SUB1A Increases ABA Responsiveness. (A) and (B) Relative mRNA levels of SUB1 genes following ABA treatment. Developmentally matched plants 14-d-old M202 versus M202(Sub1) (A) and 14-d-old LG versus 21-d-old Ubi:SUB1A-3 (B) were treated with mock (0.1% [v/v] DMSO) or ABA solution (5 or 50 μM in 0.1% [v/v] DMSO) for 24 h, and aerial tissue was analyzed by qRT-PCR (mock-treated M202 and LG = 1.0). Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between M202 versus M202(Sub1) or LG versus Ubi:SUB1A-3 (P < 0.05). (C) and (D) ABA-inhibited seed germination and shoot elongation of LG and two Ubi:SUB1A lines. Seeds were pretreated with 100 μM fluridone at 4°C for 48 h and incubated in a series of ABA solutions (0, 10, 30, or 100 μM) for 4 d (C) or 8 d (D). Relative germination (C) and relative shoot elongation (D) were calculated by comparison to the nontreated seeds of individual genotypes. Data represent mean ± sd (n = 20) from three independent biological replicates, and an asterisk indicates a significant difference between LG and Ubi:SUB1A lines (*P < 0.05; **P < 0.01). (E) The effect of fluridone on seed germination of LG and Ubi:SUB1A-3. Seeds were incubated on wet filter paper containing 0, 5, 20, or 100 μM fluridone for 0 to 6 d. Data represent mean ± sd from three independent biological replicates.
Figure 4.
Figure 4.
SUB1A Increases ABA Responsiveness at the mRNA Accumulation Level. Developmentally matched plants 14-d-old LG and 21-d-old Ubi:SUB1A-3 were treated with mock (0.1% [v/v] DMSO) or ABA solution (5 or 50 μM in 0.1% [v/v] DMSO) for 24 h, and aerial tissue was analyzed by qRT-PCR (mock-treated LG = 1.0). Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between LG and Ubi:SUB1A-3 (*P < 0.05; **P < 0.01).
Figure 5.
Figure 5.
SUB1A Moderates Dehydration Stress That Is Induced upon Desubmergence. (A) Photos of rice plants that encounter dehydration after reoxygenation. Fourteen-day-old plants were submerged for 7 d and reoxygenated for 1 h under aerobic conditions under low light (50 μmol m−2 s−1). Bars = 5 cm. (B) RWC of the youngest leaves of plants that were submerged and reoxygenated for 0 to 4 h. Data represent mean ± se (n = 8), and an asterisk indicates a significant difference between M202 and M202(Sub1) (P < 0.01). (C) Accumulation of superoxide anion and hydrogen peroxide in leaf blades upon desubmergence. Fourteen-day-old plants were completely submerged for 7 d. Immediately following desubmergence, plants were treated with NBT to detect superoxide anion or DAB to detect hydrogen peroxide in the dark for 3 and 24 h, respectively. Plants grown under aerobic conditions were used as a control. Bar = 2 cm. (D) Lipid peroxidation of aerial tissue during and after submergence. Fourteen-day-old plants were submerged for 7 d and then reoxygenated for up to 4 h. Aerial tissue was analyzed to determine the level of MDA, an end product of lipid peroxidation. Data represent mean ± sd from three independent biological replicates, and an asterisk indicates a significant difference between M202 and M202(Sub1) (P < 0.05). FW, fresh weight.
Figure 6.
Figure 6.
SUB1A Further Increases mRNA Accumulation of Genes Involved in Dehydration Tolerance after Desubmergence. Relative mRNA levels of SUB1 genes (A) and genes associated with drought response/tolerance (B). Fourteen-day-old plants were submerged for 7 d and then reoxygenated for up to 4 h. Aerial tissue was analyzed by qRT-PCR (M202 grown in air = 1.0). Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between M202 and M202(Sub1) (*P < 0.05; **P < 0.01).
Figure 7.
Figure 7.
SUB1A Enhances Tolerance to Oxidative Stress. (A) Photo of rice seedlings treated with an oxidative herbicide. Seven-day-old seedlings were transferred onto 0.5× MS media containing methyl viologen (0, 1, 5, or 20 μM) and incubated for 14 d (16 h light/8 h dark; light level, 50 μmol m−2 s−1). Bars = 3 cm. (B) Growth inhibition of aerial tissue by oxidative stress. Relative fresh weight was calculated by comparison to the nontreated seedlings of individual genotypes. Data represent mean ± sd (n = 12) from three independent biological replicates, and an asterisk indicates a significant difference between M202 and M202(Sub1) (*P < 0.05; **P < 0.01). (C) Chlorophyll (Chl) contents in aerial tissue of plants exposed to oxidative stress. Data represent mean ± sd from three independent biological replicates, and an asterisk indicates a significant difference between M202 and M202(Sub1) (*P < 0.05; **P < 0.01). FW, fresh weight. (D) Relative mRNA levels of SUB1 genes in aerial tissue of plants treated with oxidative stress. Fourteen-day-old plants were exposed to methyl viologen (0, 1, or 20 μM) for 24 h in the light (100 μmol m−2 s−1), and the aerial tissue was subjected to qRT-PCR analysis. Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between M202 versus M202(Sub1) (*P < 0.05; **P < 0.01).
Figure 8.
Figure 8.
SUB1A Further Increases mRNA Levels of Genes Associated with ROS Detoxification. Fourteen-day-old plants were exposed to methyl viologen (0, 1, or 20 μM) for 24 h in the light (100 μmol m−2 s−1), and the aerial tissue was subjected to qRT-PCR analysis. Data represent mean ± se from three independent biological replicates, and an asterisk indicates a significant difference between M202 versus M202(Sub1) (*P < 0.05; **P < 0.01).
Figure 9.
Figure 9.
Model of SUB1A-Mediated Response to the Natural Progression of Abiotic Stresses during a Flooding Event in Rice. SUB1A expression inhibits the increased GA responsiveness during submergence through elevation of the GA signaling repressors, SLR1 and SLRL1. Negative regulation of GA responses aids in avoidance of carbohydrate starvation, allowing plants to endure submergence. Upon reaeration, leaf dehydration occurs. SUB1A-mediated enhancement of ROS amelioration limits oxidative damage and chlorophyll degradation during reoxygenation. Increased ABA responsiveness by SUB1A induces expression of LEA mRNAs and suppresses leaf water loss. SUB1A also upregulates transcripts encoding ERFs associated with acclimation to drought (e.g., DREB1s and AP59). The SUB1A-mediated responses to water deficit can independently enhance recovery from submergence or provide protection during drought, both of which induce cellular dehydration.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Achard P., Cheng H., De Grauwe L., Decat J., Schoutteten H., Moritz T., Van Der Straeten D., Peng J., Harberd N.P. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science 311: 91–94 - PubMed
    1. Achard P., Renou J.-P., Berthomé R., Harberd N.P., Genschik P. (2008). Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 18: 656–660 - PubMed
    1. Acharya B.R., Assmann S.M. (2009). Hormone interactions in stomatal function. Plant Mol. Biol. 69: 451–462 - PubMed
    1. Amir Hossain M., Lee Y., Cho J.-I., Ahn C.H., Lee S.K., Jeon J.S., Kang H., Lee C.H., An G., Park P.B. (2010). The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol. Biol. 72: 557–566 - PubMed
    1. Badawi G.H., Kawano N., Yamauchi Y., Shimada E., Sasaki R., Kubo A., Tanaka K. (2004). Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol. Plant. 121: 231–238 - PubMed

Publication types

MeSH terms