Fertility of pedicellate spikelets in sorghum is controlled by a jasmonic acid regulatory module

Nicholas Gladman; Yinping Jiao; Young Koung Lee; Lifang Zhang; Ratan Chopra; Michael Regulski; Gloria Burow; Chad Hayes; Shawn A. Christensen; Lavanya Dampanaboina; Junping Chen; John Burke; Doreen Ware; Zhanguo Xin

doi:10.3390/ijms20194951

Fertility of pedicellate spikelets in sorghum is controlled by a jasmonic acid regulatory module

Nicholas Gladman, Yinping Jiao, Young Koung Lee, Lifang Zhang, Ratan Chopra, Michael Regulski, Gloria Burow, Chad Hayes, Shawn A. Christensen, Lavanya Dampanaboina, Junping Chen, John Burke, Doreen Ware, Zhanguo Xin

Agronomy and Plant Genetics

Research output: Contribution to journal › Article › peer-review

30 Scopus citations

Abstract

As in other cereal crops, the panicles of sorghum (Sorghum bicolor (L.) Moench) comprise two types of floral spikelets (grass flowers). Only sessile spikelets (SSs) are capable of producing viable grains, whereas pedicellate spikelets (PSs) cease development after initiation and eventually abort. Consequently, grain number per panicle (GNP) is lower than the total number of flowers produced per panicle. The mechanism underlying this differential fertility is not well understood. To investigate this issue, we isolated a series of ethyl methane sulfonate (EMS)-induced multiseeded (msd) mutants that result in full spikelet fertility, effectively doubling GNP. Previously, we showed that MSD1 is a TCP (Teosinte branched/Cycloidea/PCF) transcription factor that regulates jasmonic acid (JA) biosynthesis, and ultimately floral sex organ development. Here, we show that MSD2 encodes a lipoxygenase (LOX) that catalyzes the first committed step of JA biosynthesis. Further, we demonstrate that MSD1 binds to the promoters of MSD2 and other JA pathway genes. Together, these results show that a JA-induced module regulates sorghum panicle development and spikelet fertility. The findings advance our understanding of inflorescence development and could lead to new strategies for increasing GNP and grain yield in sorghum and other cereal crops.

Original language	English (US)
Article number	4951
Journal	International journal of molecular sciences
Volume	20
Issue number	19
DOIs	https://doi.org/10.3390/ijms20194951
State	Published - Oct 1 2019

Bibliographical note

Funding Information:
Funding: N.G., Y.J., R.C., G.B., J.B., C.H., and Z.X. acknowledge support from the United Sorghum Checkoff program. Z.X. was also partly supported by USDA ARS 3096-21000-019-00-D. Y.J., Y.K.L., N.G., M.R., and D.W. were partly supported by USDA ARS 8062-21000-041-00D. Y.K.L. acknowledges that this work was supported by a grant from the Next-Generation BioGreen 21 Program (Project No. PJ013658032019), Rural Development Administration, Republic of Korea, and R&D Program of ‘Plasma Advanced Technology for Agriculture and Food (Plasma Farming)’ through the National Fusion Research Institute of Korea (NFRI). NG was supported by an ARS-funded postdoc fellowship. The APC was funded by USDA ARS 8062-21000-041-00D.

Funding Information:
N.G., Y.J., R.C., G.B., J.B., C.H., and Z.X. acknowledge support from the United Sorghum Checkoff program. Z.X. was also partly supported by USDA ARS 3096-21000-019-00-D. Y.J., Y.K.L., N.G., M.R., and D.W. were partly supported by USDA ARS 8062-21000-041-00D. Y.K.L. acknowledges that this work was supported by a grant from the Next-Generation BioGreen 21 Program (Project No. PJ013658032019), Rural Development Administration, Republic of Korea, and R&D Program of ?Plasma Advanced Technology for Agriculture and Food (Plasma Farming)? through the National Fusion Research Institute of Korea (NFRI). NG was supported by an ARS-funded postdoc fellowship. The APC was funded by USDA ARS 8062-21000-041-00D. Acknowledgments: The authors wish to thank all the support staff, students, and farmers that have made this work possible.

Publisher Copyright:
© 2019 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Gene expression
Jasmonic acid signaling
Plant development
Transcriptional regulators

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Gladman, N., Jiao, Y., Lee, Y. K., Zhang, L., Chopra, R., Regulski, M., Burow, G., Hayes, C., Christensen, S. A., Dampanaboina, L., Chen, J., Burke, J., Ware, D., & Xin, Z. (2019). Fertility of pedicellate spikelets in sorghum is controlled by a jasmonic acid regulatory module. International journal of molecular sciences, 20(19), Article 4951. https://doi.org/10.3390/ijms20194951

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abstract = "As in other cereal crops, the panicles of sorghum (Sorghum bicolor (L.) Moench) comprise two types of floral spikelets (grass flowers). Only sessile spikelets (SSs) are capable of producing viable grains, whereas pedicellate spikelets (PSs) cease development after initiation and eventually abort. Consequently, grain number per panicle (GNP) is lower than the total number of flowers produced per panicle. The mechanism underlying this differential fertility is not well understood. To investigate this issue, we isolated a series of ethyl methane sulfonate (EMS)-induced multiseeded (msd) mutants that result in full spikelet fertility, effectively doubling GNP. Previously, we showed that MSD1 is a TCP (Teosinte branched/Cycloidea/PCF) transcription factor that regulates jasmonic acid (JA) biosynthesis, and ultimately floral sex organ development. Here, we show that MSD2 encodes a lipoxygenase (LOX) that catalyzes the first committed step of JA biosynthesis. Further, we demonstrate that MSD1 binds to the promoters of MSD2 and other JA pathway genes. Together, these results show that a JA-induced module regulates sorghum panicle development and spikelet fertility. The findings advance our understanding of inflorescence development and could lead to new strategies for increasing GNP and grain yield in sorghum and other cereal crops.",

keywords = "Gene expression, Jasmonic acid signaling, Plant development, Transcriptional regulators",

author = "Nicholas Gladman and Yinping Jiao and Lee, {Young Koung} and Lifang Zhang and Ratan Chopra and Michael Regulski and Gloria Burow and Chad Hayes and Christensen, {Shawn A.} and Lavanya Dampanaboina and Junping Chen and John Burke and Doreen Ware and Zhanguo Xin",

note = "Funding Information: Funding: N.G., Y.J., R.C., G.B., J.B., C.H., and Z.X. acknowledge support from the United Sorghum Checkoff program. Z.X. was also partly supported by USDA ARS 3096-21000-019-00-D. Y.J., Y.K.L., N.G., M.R., and D.W. were partly supported by USDA ARS 8062-21000-041-00D. Y.K.L. acknowledges that this work was supported by a grant from the Next-Generation BioGreen 21 Program (Project No. PJ013658032019), Rural Development Administration, Republic of Korea, and R&D Program of {\textquoteleft}Plasma Advanced Technology for Agriculture and Food (Plasma Farming){\textquoteright} through the National Fusion Research Institute of Korea (NFRI). NG was supported by an ARS-funded postdoc fellowship. The APC was funded by USDA ARS 8062-21000-041-00D. Funding Information: N.G., Y.J., R.C., G.B., J.B., C.H., and Z.X. acknowledge support from the United Sorghum Checkoff program. Z.X. was also partly supported by USDA ARS 3096-21000-019-00-D. Y.J., Y.K.L., N.G., M.R., and D.W. were partly supported by USDA ARS 8062-21000-041-00D. Y.K.L. acknowledges that this work was supported by a grant from the Next-Generation BioGreen 21 Program (Project No. PJ013658032019), Rural Development Administration, Republic of Korea, and R&D Program of ?Plasma Advanced Technology for Agriculture and Food (Plasma Farming)? through the National Fusion Research Institute of Korea (NFRI). NG was supported by an ARS-funded postdoc fellowship. The APC was funded by USDA ARS 8062-21000-041-00D. Acknowledgments: The authors wish to thank all the support staff, students, and farmers that have made this work possible. Publisher Copyright: {\textcopyright} 2019 by the authors. Licensee MDPI, Basel, Switzerland.",

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AU - Jiao, Yinping

AU - Lee, Young Koung

AU - Zhang, Lifang

AU - Chopra, Ratan

AU - Regulski, Michael

AU - Burow, Gloria

AU - Hayes, Chad

AU - Christensen, Shawn A.

AU - Dampanaboina, Lavanya

AU - Chen, Junping

AU - Burke, John

AU - Ware, Doreen

AU - Xin, Zhanguo

N1 - Funding Information: Funding: N.G., Y.J., R.C., G.B., J.B., C.H., and Z.X. acknowledge support from the United Sorghum Checkoff program. Z.X. was also partly supported by USDA ARS 3096-21000-019-00-D. Y.J., Y.K.L., N.G., M.R., and D.W. were partly supported by USDA ARS 8062-21000-041-00D. Y.K.L. acknowledges that this work was supported by a grant from the Next-Generation BioGreen 21 Program (Project No. PJ013658032019), Rural Development Administration, Republic of Korea, and R&D Program of ‘Plasma Advanced Technology for Agriculture and Food (Plasma Farming)’ through the National Fusion Research Institute of Korea (NFRI). NG was supported by an ARS-funded postdoc fellowship. The APC was funded by USDA ARS 8062-21000-041-00D. Funding Information: N.G., Y.J., R.C., G.B., J.B., C.H., and Z.X. acknowledge support from the United Sorghum Checkoff program. Z.X. was also partly supported by USDA ARS 3096-21000-019-00-D. Y.J., Y.K.L., N.G., M.R., and D.W. were partly supported by USDA ARS 8062-21000-041-00D. Y.K.L. acknowledges that this work was supported by a grant from the Next-Generation BioGreen 21 Program (Project No. PJ013658032019), Rural Development Administration, Republic of Korea, and R&D Program of ?Plasma Advanced Technology for Agriculture and Food (Plasma Farming)? through the National Fusion Research Institute of Korea (NFRI). NG was supported by an ARS-funded postdoc fellowship. The APC was funded by USDA ARS 8062-21000-041-00D. Acknowledgments: The authors wish to thank all the support staff, students, and farmers that have made this work possible. Publisher Copyright: © 2019 by the authors. Licensee MDPI, Basel, Switzerland.

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N2 - As in other cereal crops, the panicles of sorghum (Sorghum bicolor (L.) Moench) comprise two types of floral spikelets (grass flowers). Only sessile spikelets (SSs) are capable of producing viable grains, whereas pedicellate spikelets (PSs) cease development after initiation and eventually abort. Consequently, grain number per panicle (GNP) is lower than the total number of flowers produced per panicle. The mechanism underlying this differential fertility is not well understood. To investigate this issue, we isolated a series of ethyl methane sulfonate (EMS)-induced multiseeded (msd) mutants that result in full spikelet fertility, effectively doubling GNP. Previously, we showed that MSD1 is a TCP (Teosinte branched/Cycloidea/PCF) transcription factor that regulates jasmonic acid (JA) biosynthesis, and ultimately floral sex organ development. Here, we show that MSD2 encodes a lipoxygenase (LOX) that catalyzes the first committed step of JA biosynthesis. Further, we demonstrate that MSD1 binds to the promoters of MSD2 and other JA pathway genes. Together, these results show that a JA-induced module regulates sorghum panicle development and spikelet fertility. The findings advance our understanding of inflorescence development and could lead to new strategies for increasing GNP and grain yield in sorghum and other cereal crops.

AB - As in other cereal crops, the panicles of sorghum (Sorghum bicolor (L.) Moench) comprise two types of floral spikelets (grass flowers). Only sessile spikelets (SSs) are capable of producing viable grains, whereas pedicellate spikelets (PSs) cease development after initiation and eventually abort. Consequently, grain number per panicle (GNP) is lower than the total number of flowers produced per panicle. The mechanism underlying this differential fertility is not well understood. To investigate this issue, we isolated a series of ethyl methane sulfonate (EMS)-induced multiseeded (msd) mutants that result in full spikelet fertility, effectively doubling GNP. Previously, we showed that MSD1 is a TCP (Teosinte branched/Cycloidea/PCF) transcription factor that regulates jasmonic acid (JA) biosynthesis, and ultimately floral sex organ development. Here, we show that MSD2 encodes a lipoxygenase (LOX) that catalyzes the first committed step of JA biosynthesis. Further, we demonstrate that MSD1 binds to the promoters of MSD2 and other JA pathway genes. Together, these results show that a JA-induced module regulates sorghum panicle development and spikelet fertility. The findings advance our understanding of inflorescence development and could lead to new strategies for increasing GNP and grain yield in sorghum and other cereal crops.

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ER -

Fertility of pedicellate spikelets in sorghum is controlled by a jasmonic acid regulatory module

Abstract

Bibliographical note

Keywords

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