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Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage

BACKGROUND: Decreased spikelet fertility is often responsible for reduction in grain yield in rice (Oryza sativa L.). In this study, two varieties with different levels of heat tolerance, Liangyoupeijiu (LYPJ, heat susceptible) and Shanyou63 (SY63, heat tolerant) were subjected to two temperature tr...

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Autores principales: Hu, Qiuqian, Wang, Wencheng, Lu, Qifan, Huang, Jianliang, Peng, Shaobing, Cui, Kehui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8451141/
https://www.ncbi.nlm.nih.gov/pubmed/34544370
http://dx.doi.org/10.1186/s12870-021-03209-w
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author Hu, Qiuqian
Wang, Wencheng
Lu, Qifan
Huang, Jianliang
Peng, Shaobing
Cui, Kehui
author_facet Hu, Qiuqian
Wang, Wencheng
Lu, Qifan
Huang, Jianliang
Peng, Shaobing
Cui, Kehui
author_sort Hu, Qiuqian
collection PubMed
description BACKGROUND: Decreased spikelet fertility is often responsible for reduction in grain yield in rice (Oryza sativa L.). In this study, two varieties with different levels of heat tolerance, Liangyoupeijiu (LYPJ, heat susceptible) and Shanyou63 (SY63, heat tolerant) were subjected to two temperature treatments for 28 days during the panicle initiation stage in temperature/relative humidity-controlled greenhouses: high temperature (HT; 37/27 °C; day/night) and control temperature (CK; 31/27 °C; day/night) to investigate changes in anther development under HT during panicle initiation and their relationship with spikelet fertility. RESULTS: HT significantly decreased the grain yield of LYPJ by decreasing the number of spikelets per panicle and seed setting percentage. In addition, HT produced minor adverse effects in SY63. The decreased spikelet fertility was primarily attributed to decreased pollen viability and anther dehiscence, as well as poor pollen shedding of the anthers of LYPJ under HT. HT resulted in abnormal anther development (fewer vacuolated microspores, un-degraded tapetum, unevenly distributed Ubisch bodies) and malformation of pollen (obscure outline of the pollen exine with a collapsed bacula, disordered tectum, and no nexine of the pollen walls, uneven sporopollenin deposition on the surface of pollen grains) in LYPJ, which may have lowered pollen viability. Additionally, HT produced a compact knitted anther cuticle structure of the epidermis, an un-degraded septum, a thickened anther wall, unevenly distributed Ubisch bodies, and inhibition of the confluent locule, and these malformed structures may be partially responsible for the decreased anther dehiscence rate and reduced pollen shedding of the anthers in LYPJ. In contrast, the anther wall and pollen development of SY63 were not substantially changed under HT. CONCLUSIONS: Our results suggest that disturbed anther walls and pollen development are responsible for the reduced spikelet fertility and grain yield of the tested heat susceptible variety, and noninvasive anthers and pollen formation in response to HT were associated with improved heat tolerance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03209-w.
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spelling pubmed-84511412021-09-20 Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage Hu, Qiuqian Wang, Wencheng Lu, Qifan Huang, Jianliang Peng, Shaobing Cui, Kehui BMC Plant Biol Research Article BACKGROUND: Decreased spikelet fertility is often responsible for reduction in grain yield in rice (Oryza sativa L.). In this study, two varieties with different levels of heat tolerance, Liangyoupeijiu (LYPJ, heat susceptible) and Shanyou63 (SY63, heat tolerant) were subjected to two temperature treatments for 28 days during the panicle initiation stage in temperature/relative humidity-controlled greenhouses: high temperature (HT; 37/27 °C; day/night) and control temperature (CK; 31/27 °C; day/night) to investigate changes in anther development under HT during panicle initiation and their relationship with spikelet fertility. RESULTS: HT significantly decreased the grain yield of LYPJ by decreasing the number of spikelets per panicle and seed setting percentage. In addition, HT produced minor adverse effects in SY63. The decreased spikelet fertility was primarily attributed to decreased pollen viability and anther dehiscence, as well as poor pollen shedding of the anthers of LYPJ under HT. HT resulted in abnormal anther development (fewer vacuolated microspores, un-degraded tapetum, unevenly distributed Ubisch bodies) and malformation of pollen (obscure outline of the pollen exine with a collapsed bacula, disordered tectum, and no nexine of the pollen walls, uneven sporopollenin deposition on the surface of pollen grains) in LYPJ, which may have lowered pollen viability. Additionally, HT produced a compact knitted anther cuticle structure of the epidermis, an un-degraded septum, a thickened anther wall, unevenly distributed Ubisch bodies, and inhibition of the confluent locule, and these malformed structures may be partially responsible for the decreased anther dehiscence rate and reduced pollen shedding of the anthers in LYPJ. In contrast, the anther wall and pollen development of SY63 were not substantially changed under HT. CONCLUSIONS: Our results suggest that disturbed anther walls and pollen development are responsible for the reduced spikelet fertility and grain yield of the tested heat susceptible variety, and noninvasive anthers and pollen formation in response to HT were associated with improved heat tolerance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03209-w. BioMed Central 2021-09-20 /pmc/articles/PMC8451141/ /pubmed/34544370 http://dx.doi.org/10.1186/s12870-021-03209-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Hu, Qiuqian
Wang, Wencheng
Lu, Qifan
Huang, Jianliang
Peng, Shaobing
Cui, Kehui
Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage
title Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage
title_full Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage
title_fullStr Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage
title_full_unstemmed Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage
title_short Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage
title_sort abnormal anther development leads to lower spikelet fertility in rice (oryza sativa l.) under high temperature during the panicle initiation stage
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8451141/
https://www.ncbi.nlm.nih.gov/pubmed/34544370
http://dx.doi.org/10.1186/s12870-021-03209-w
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