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Ozone-Induced Rice Grain Yield Loss Is Triggered via a Change in Panicle Morphology That Is Controlled by ABERRANT PANICLE ORGANIZATION 1 Gene.

Tsukahara K, Sawada H, Kohno Y, Matsuura T, Mori IC, Terao T, Ioki M, Tamaoki M - PLoS ONE (2015)

Bottom Line: The Habataki allele of the APO1 locus in a near-isogenic line also resulted in grain yield loss upon ozone exposure, suggesting APO1 involvement in ozone-induced yield loss.Only a few differences in the APO1 amino acid sequences were detected between the cultivars, but the APO1 transcript level was oppositely regulated by ozone exposure: i.e., it increased in Sasanishiki and decreased in Habataki.These data indicate that ozone-induced grain yield loss in Habataki is caused by a reduction in the APO1 transcript level through an increase in the levels of phytohormones that reduce leaf damage.

View Article: PubMed Central - PubMed

Affiliation: Center for Environmental Biology and Ecosystem, National Institute for Environmental Studies, Tsukuba, Ibaraki, 305-8506, Japan; Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8577, Japan.

ABSTRACT
Rice grain yield is predicted to decrease in the future because of an increase in tropospheric ozone concentration. However, the underlying mechanisms are unclear. Here, we investigated the responses to ozone of two rice (Oryza Sativa L.) cultivars, Sasanishiki and Habataki. Sasanishiki showed ozone-induced leaf injury, but no grain yield loss. By contrast, Habataki showed grain yield loss with minimal leaf injury. A QTL associated with grain yield loss caused by ozone was identified in Sasanishiki/Habataki chromosome segment substitution lines and included the ABERRANT PANICLE ORGANIZATION 1 (APO1) gene. The Habataki allele of the APO1 locus in a near-isogenic line also resulted in grain yield loss upon ozone exposure, suggesting APO1 involvement in ozone-induced yield loss. Only a few differences in the APO1 amino acid sequences were detected between the cultivars, but the APO1 transcript level was oppositely regulated by ozone exposure: i.e., it increased in Sasanishiki and decreased in Habataki. Interestingly, the levels of some phytohormones (jasmonic acid, jasmonoyl-L-isoleucine, and abscisic acid) known to be involved in attenuation of ozone-induced leaf injury tended to decrease in Sasanishiki but to increase in Habataki upon ozone exposure. These data indicate that ozone-induced grain yield loss in Habataki is caused by a reduction in the APO1 transcript level through an increase in the levels of phytohormones that reduce leaf damage.

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Effects of the Habataki-type APO1 gene in Habataki and the SHA422-1.1 near-isogenic line.(A) Graphical genotype of chromosome 6 of SHA422-1.1 (APO1 near-isogenic line) and SHA422-1.3. The thickest arrow represents the open reading frame of APO1; narrower arrows represent other predicted genes. 1.1, SHA422-1.1; 1.3, SHA422-1.3. Modified from [20]. (B, C) Effects of the Habataki-type APO1 gene on (B) grain yield and (C) the number of primary rachis branches. Values are mean ± SD (n = 36). NF, non-filtered air (converted values); O3, elevated ozone. Bars topped by the same letters are not significantly different (Tukey’s HSD test, P<0.05).
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pone.0123308.g004: Effects of the Habataki-type APO1 gene in Habataki and the SHA422-1.1 near-isogenic line.(A) Graphical genotype of chromosome 6 of SHA422-1.1 (APO1 near-isogenic line) and SHA422-1.3. The thickest arrow represents the open reading frame of APO1; narrower arrows represent other predicted genes. 1.1, SHA422-1.1; 1.3, SHA422-1.3. Modified from [20]. (B, C) Effects of the Habataki-type APO1 gene on (B) grain yield and (C) the number of primary rachis branches. Values are mean ± SD (n = 36). NF, non-filtered air (converted values); O3, elevated ozone. Bars topped by the same letters are not significantly different (Tukey’s HSD test, P<0.05).

Mentions: The highest LOD scores for grain yield and the number of primary rachis branches in 2009 and 2010 were at the RM3430 marker (107.6 cM on chromosome 6; Figs 2 and 3). These results suggest that genes near RM3430 play key roles in grain yield loss by decreasing the number of primary rachis branches under elevated ozone. Our previous study showed that RM3430 lies close to the ABERRANT PANICLE ORGANIZATION 1 (APO1) gene [18]. The gene encodes an F-box protein [34] and is known to affect rice grain yield through regulation of primary rachis branch formation [20]. To investigate whether the APO1 allele in Habataki is involved in the decrease in grain yield and in the number of primary rachis branches, we carried out an ozone exposure experiment with SHA422-1.1, a near isogenic line derived from a CSSL that has only the Habataki-genotype APO1 region in the Sasanishiki background (Fig 4A). As a control, we also used SHA422-1.3, a sib line of SHA422-1.1 that almost all region of chromosome have the Sasanishiki genotype. Grain yield and plant growth parameters of SHA422-1.1, SHA422-1.3, Sasanishiki and Habataki grown in the open-top chambers with elevated or low (charcoal-filtered air) ozone were measured (Fig 4B, 4C and Table E in S1 File). Grain yield and the number of primary rachis branches decreased significantly under elevated ozone in all of three lines, except grain yield of SHA422-1.1 (P = 0.059, Fig 4B and 4C). Both grain yield and the number of primary rachis branches decreased significantly under elevated ozone in SHA422-1.1 and Habataki (P<0.05, Fig 4B and 4C). These results indicate that the Habataki allele of APO1 is involved in the reduction of grain yield and of the number of primary rachis branches by ozone.


Ozone-Induced Rice Grain Yield Loss Is Triggered via a Change in Panicle Morphology That Is Controlled by ABERRANT PANICLE ORGANIZATION 1 Gene.

Tsukahara K, Sawada H, Kohno Y, Matsuura T, Mori IC, Terao T, Ioki M, Tamaoki M - PLoS ONE (2015)

Effects of the Habataki-type APO1 gene in Habataki and the SHA422-1.1 near-isogenic line.(A) Graphical genotype of chromosome 6 of SHA422-1.1 (APO1 near-isogenic line) and SHA422-1.3. The thickest arrow represents the open reading frame of APO1; narrower arrows represent other predicted genes. 1.1, SHA422-1.1; 1.3, SHA422-1.3. Modified from [20]. (B, C) Effects of the Habataki-type APO1 gene on (B) grain yield and (C) the number of primary rachis branches. Values are mean ± SD (n = 36). NF, non-filtered air (converted values); O3, elevated ozone. Bars topped by the same letters are not significantly different (Tukey’s HSD test, P<0.05).
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pone.0123308.g004: Effects of the Habataki-type APO1 gene in Habataki and the SHA422-1.1 near-isogenic line.(A) Graphical genotype of chromosome 6 of SHA422-1.1 (APO1 near-isogenic line) and SHA422-1.3. The thickest arrow represents the open reading frame of APO1; narrower arrows represent other predicted genes. 1.1, SHA422-1.1; 1.3, SHA422-1.3. Modified from [20]. (B, C) Effects of the Habataki-type APO1 gene on (B) grain yield and (C) the number of primary rachis branches. Values are mean ± SD (n = 36). NF, non-filtered air (converted values); O3, elevated ozone. Bars topped by the same letters are not significantly different (Tukey’s HSD test, P<0.05).
Mentions: The highest LOD scores for grain yield and the number of primary rachis branches in 2009 and 2010 were at the RM3430 marker (107.6 cM on chromosome 6; Figs 2 and 3). These results suggest that genes near RM3430 play key roles in grain yield loss by decreasing the number of primary rachis branches under elevated ozone. Our previous study showed that RM3430 lies close to the ABERRANT PANICLE ORGANIZATION 1 (APO1) gene [18]. The gene encodes an F-box protein [34] and is known to affect rice grain yield through regulation of primary rachis branch formation [20]. To investigate whether the APO1 allele in Habataki is involved in the decrease in grain yield and in the number of primary rachis branches, we carried out an ozone exposure experiment with SHA422-1.1, a near isogenic line derived from a CSSL that has only the Habataki-genotype APO1 region in the Sasanishiki background (Fig 4A). As a control, we also used SHA422-1.3, a sib line of SHA422-1.1 that almost all region of chromosome have the Sasanishiki genotype. Grain yield and plant growth parameters of SHA422-1.1, SHA422-1.3, Sasanishiki and Habataki grown in the open-top chambers with elevated or low (charcoal-filtered air) ozone were measured (Fig 4B, 4C and Table E in S1 File). Grain yield and the number of primary rachis branches decreased significantly under elevated ozone in all of three lines, except grain yield of SHA422-1.1 (P = 0.059, Fig 4B and 4C). Both grain yield and the number of primary rachis branches decreased significantly under elevated ozone in SHA422-1.1 and Habataki (P<0.05, Fig 4B and 4C). These results indicate that the Habataki allele of APO1 is involved in the reduction of grain yield and of the number of primary rachis branches by ozone.

Bottom Line: The Habataki allele of the APO1 locus in a near-isogenic line also resulted in grain yield loss upon ozone exposure, suggesting APO1 involvement in ozone-induced yield loss.Only a few differences in the APO1 amino acid sequences were detected between the cultivars, but the APO1 transcript level was oppositely regulated by ozone exposure: i.e., it increased in Sasanishiki and decreased in Habataki.These data indicate that ozone-induced grain yield loss in Habataki is caused by a reduction in the APO1 transcript level through an increase in the levels of phytohormones that reduce leaf damage.

View Article: PubMed Central - PubMed

Affiliation: Center for Environmental Biology and Ecosystem, National Institute for Environmental Studies, Tsukuba, Ibaraki, 305-8506, Japan; Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8577, Japan.

ABSTRACT
Rice grain yield is predicted to decrease in the future because of an increase in tropospheric ozone concentration. However, the underlying mechanisms are unclear. Here, we investigated the responses to ozone of two rice (Oryza Sativa L.) cultivars, Sasanishiki and Habataki. Sasanishiki showed ozone-induced leaf injury, but no grain yield loss. By contrast, Habataki showed grain yield loss with minimal leaf injury. A QTL associated with grain yield loss caused by ozone was identified in Sasanishiki/Habataki chromosome segment substitution lines and included the ABERRANT PANICLE ORGANIZATION 1 (APO1) gene. The Habataki allele of the APO1 locus in a near-isogenic line also resulted in grain yield loss upon ozone exposure, suggesting APO1 involvement in ozone-induced yield loss. Only a few differences in the APO1 amino acid sequences were detected between the cultivars, but the APO1 transcript level was oppositely regulated by ozone exposure: i.e., it increased in Sasanishiki and decreased in Habataki. Interestingly, the levels of some phytohormones (jasmonic acid, jasmonoyl-L-isoleucine, and abscisic acid) known to be involved in attenuation of ozone-induced leaf injury tended to decrease in Sasanishiki but to increase in Habataki upon ozone exposure. These data indicate that ozone-induced grain yield loss in Habataki is caused by a reduction in the APO1 transcript level through an increase in the levels of phytohormones that reduce leaf damage.

Show MeSH
Related in: MedlinePlus