Two rice MYB transcription factors maintain male fertility in response to photoperiod by modulating sugar partitioning.
CARBON STARVED ANTHER
MYB transcription factor
anther development
floral initiation
photoperiod
rice
sugar partitioning
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
16
12
2020
accepted:
05
05
2021
pubmed:
26
5
2021
medline:
22
7
2021
entrez:
25
5
2021
Statut:
ppublish
Résumé
Photoperiod-dependent male fertility is a critical enabler of modern hybrid breeding. A MYB transcription factor, CSA, is a key regulator of sugar partitioning in rice anthers, disruption of which causes photoperiod-sensitive male sterility. However, little is known about the molecular mechanisms governing plant fertility in response to photoperiod. Here, we have obtained another rice photoperiod-sensitive male sterile mutant, csa2, which exhibits semi-sterility under long-day (LD) conditions, with normal fertility under short-day (SD) conditions. CSA2 specifically expressed in anthers, and here is shown to be indispensable for sugar partitioning to anthers under LD conditions. The CSA2 protein can restore the fertility of csa mutants under SD conditions when expressed in a CSA-specific pattern, indicating that the two proteins share common downstream regulatory targets. Transcriptomic analyses also reveal discrete regulatory targets in anthers. Furthermore, the regulatory role of CSA2 in sugar transport was influenced by the photoperiod conditions during floral initiation, not simply during anther development. Collectively, we propose that rice evolved at least two MYB proteins, CSA2 and CSA, that regulate sugar transport in anthers under LD and SD conditions, respectively. This finding provides insight into the molecular mechanisms that regulate male fertility in response to photoperiod.
Substances chimiques
Plant Proteins
0
Sugars
0
Transcription Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1612-1629Informations de copyright
© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.
Références
Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13: 627-639.
Aya K, Tanaka MU, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M. 2009. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21: 1453-1472.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statal Society: Series B (Methodological) 57: 289-300.
Blümel M, Dally N, Jung C. 2015. Flowering time regulation in crops - what did we learn from Arabidopsis? Current Opinion in Biotechnology 32: 121-129.
Braun DM, Wang L, Ruan YL. 2014. Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. Journal of Experimental Botany 65: 1713-1735.
Cakmak I, Yazici AM. 2010. Magnesium: a forgotten element in crop production. Better Crops 94: 23-25.
Cheng Z. 2013. Analyzing meiotic chromosomes in rice. In: Pawlowski WP, Grelon M, Armstrong S, eds. Plant Meiosis. Berlin, German: Springer, 125-134.
Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EAR, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C et al. 2007. Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Functional and Integrative Genomics 7: 111-134.
Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q. 2012a. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proceedings of the National Academy of Sciences, USA 109: 2654-2659.
Ding J, Shen J, Mao H, Xie W, Li X, Zhang Q. 2012b. RNA-directed DNA methylation is involved in regulating photoperiod- sensitive male sterility in rice. Molecular Plant 5: 1210-1216.
Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R. 2007. A systems biology approach for pathway level analysis. Genome Research 17: 1537-1545.
Fan Y, Yang J, Mathioni SM, Yu J, Shen J, Yang X, Wang L, Zhang Q, Cai Z, Xu C et al. 2016. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proceedings of the National Academy of Sciences, USA 113: 15144-15149.
Goetz M, Godt De, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T. 2001. Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proceedings of the National Academy of Sciences, USA 98: 6522-6527.
Gross BL, Zhao Z. 2014. Archaeological and genetic insights into the origins of domesticated rice. Proceedings of the National Academy of Sciences, USA 111: 6190-6197.
Hammond JP, White PJ. 2008. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. Journal of Experimental Botany 59: 93-109.
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. 2003. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422: 719-722.
Hiei Y, Komari T, Kubo T. 1997. Transformation of rice mediated by Agrobacterium tumefaciens. Plant Molecular Biology 35: 205-218.
Huang X, Kurata N, Wei X, Wang Z-X, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W et al. 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature 490: 497-501.
Jia L, Zhang B, Mao C, Li J, Wu Y, Wu P, Wu Z. 2008. OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 228: 51-59.
Johnson DA, Thomas MA. 2007. The monosaccharide transporter gene family in Arabidopsis and rice: a history of duplications, adaptive evolution, and functional divergence. Molecular Biology and Evolution 24: 2412-2423.
Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T, Sano N, Koshiba T, Kamiya Y, Ueda M, Seo M. 2016. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nature Communications 7: 1-11.
Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC. 2012. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13: 544-562.
Kim YJ, Zhang D. 2018. Molecular control of male fertility for crop hybrid breeding. Trends in Plant Science 23: 53-65.
Komiya R, Yokoi S, Shimamoto K. 2009. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136: 3443-3450.
Kouchi H, Hata S. 1993. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. MGG Molecular & General Genetics 238: 106-119.
Kretzschmar T, Pelayo MAF, Trijatmiko KR, Gabunada LFM, Alam R, Jimenez R, Mendioro MS, Slamet-Loedin IH, Sreenivasulu N, Bailey-Serres J et al. 2015. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nature Plants 1: 1-5.
Lemoine R, Camera SL, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J-L, Laloi M, Coutos-Thévenot P, Maurousset L et al. 2013. Source-to-sink transport of sugar and regulation by environmental factors. Frontiers in Plant Science 4: 1-21.
Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J et al. 2006. The rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999-3014.
Li Q, Zhang D, Chen M, Liang W, Wei J, Qi Y, Yuan Z. 2016. Development of japonica photo-sensitive genic male sterile rice lines by editing Carbon Starved Anther Using CRISPR/Cas9. Journal of Genetics and Genomics 43: 415-419.
Li WP, Zhang WL, Tian ZM, Huang S, Zhao WM. 2004. Breeding strategy of male sterile maize line with thermo-photoperiod sensitivity. Acta Bota. Boreal-Occident. Sin. 24: 488-493.
Li YM, Forney C, Bondada B, Leng F, Sen XZ. 2021. The molecular regulation of carbon sink strength in grapevine (Vitis vinifera L.). Frontiers in Plant Science 11: 1-14.
Liu Z, Bao W, Liang W, Yin J, Zhang D. 2010. Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. Journal of Integrative Plant Biology 52: 670-678.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 1-21.
Ma J, Wei H, Liu J, Song M, Pang C, Wang L, Zhang W, Fan S, Yu S. 2013. Selection and characterization of a novel photoperiod-sensitive male sterile line in upland cotton. Journal of Integrative Plant Biology 55: 608-618.
Mamun EA, Cantrill LC, Overall RL, Sutton BG. 2005. Cellular organisation in meiotic and early post-meiotic rice anthers. Cell Biology International 29: 903-913.
Marschner H, Kirkby EA, Cakmak I. 1996. Effect of mineral nutritional status on shoot-root partitioning of photoassimilates and cycling of mineral nutrients. Journal of Experimental Botany 47: 1255-1263.
Millar AA, Gubler F. 2005. The Arabidopsis GAMYB-like Genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705-721.
Murray F, Kalla R, Jacobsen J, Gubler F. 2003. A role for HvGAMYB in anther development. The Plant Journal 33: 481-491.
Nakano H, Makino A, Mae T. 1995. Effects of panicle removal on the photosynthetic characteristics of the flag leaf of rice plants during the ripening stage. Plant and Cell Physiology 36: 653-659.
Nakano H, Muramatsu S, Makino A, Mae T. 2000. Relationship between the suppression of photosynthesis and starch accumulation in the pod-removed bean. Functional Plant Biology 27: 167-173.
Nebauer SG, Renau-Morata B, Guardiola JL, Molina RV, Pereira J. 2011. Photosynthesis down-regulation precedes carbohydrate accumulation under sink limitation in Citrus. Tree Physiology 31: 169-177.
Pacini E. 1996. Types and meaning of pollen carbohydrate reserves. Sexual Plant Reproduction 9: 362-366.
Pinheiro C, Rodrigues AP, De Carvalho IS, Chaves MM, Ricardo CP. 2005. Sugar metabolism in developing lupin seeds is affected by a short-term water deficit. Journal of Experimental Botany 56: 2705-2712.
Proietti P, Nasini L, Famiani F. 2006. Effect of different leaf-to-fruit ratios on photosynthesis and fruit growth in olive (Olea europaea L.). Photosynthetica 44: 275-285.
Radice S, Ontivero M, Giordani E, Bellini E. 2008. Anatomical differences on development of fertile and sterile pollen grains of Prunus salicina Lindl. Plant Systematics and Evolution 273: 63-69.
Sawhney VK. 2004. Photoperiod-sensitive male-sterile mutant in tomato and its potential use in hybrid seed production. Journal of Horticultural Science and Biotechnology 79: 138-141.
Scofield GN, Hirose T, Aoki N, Furbank RT. 2007. Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. Journal of Experimental Botany 58: 3155-3169.
Serrano-Bueno G, Romero-Campero FJ, Lucas-Reina E, Romero JM, Valverde F. 2017. Evolution of photoperiod sensing in plants and algae. Current Opinion in Plant Biology 37: 10-17.
Sun MX, Huang XY, Yang J, Guan YF, Yang ZN. 2013. Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Plant Reproduction 26: 83-91.
Suwa R, Hakata H, Hara H, El-Shemy HA, Adu-Gyamfi JJ, Nguyen NT, Kanai S, Lightfoot DA, Mohapatra PK, Fujita K. 2010. High temperature effects on photosynthate partitioning and sugar metabolism during ear expansion in maize (Zea mays L.) genotypes. Plant Physiology and Biochemistry 48: 124-130.
Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H et al. 2006. GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. The Plant Journal 47: 427-444.
Urban L, Léchaudel M, Lu P. 2004. Effect of fruit load and girdling on leaf photosynthesis in Mangifera indica L. Journal of Experimental Botany 55: 2075-2085.
Vaast P, Angrand J, Franck N, Dauzat J, Génard M. 2005. Fruit load and branch ring-barking affect carbon allocation and photosynthesis of leaf and fruit of Coffea arabica in the field. Tree Physiology 25: 753-760.
Wang XY, Yu CH, Li X, Wang CY, Zheng GC. 2004. Ultrastructural aspects and possible origin of cytoplasmic channels providing intercellular connection in vegetative tissues of anthers. Russian Journal of Plant Physiology 51: 97-106.
Watanabe T, Kitagawa H. 2000. Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Homoptera: Delphacidae). Journal of Economic Entomology 93: 1192-1198.
Woodward FI. 2002. Potential impacts of global elevated CO2 concentrations on plants. Current Opinion in Plant Biology 5: 207-211.
Xue Z, Xu X, Zhou Y, Wang X, Zhang Y, Liu D, Zhao B, Duan L, Qi X. 2018. Deficiency of a triterpene pathway results in humidity-sensitive genic male sterility in rice. Nature Communications 9: 1-10.
Yang S, Cheng B, Shen W, Xia J. 2009. Progress of application and breeding on two-line hybrid rice in China. Hybrid Rice. 24: 5-9.
Yu J, Han J, Kim Y-J, Song M, Yang Z, He Yi, Fu R, Luo Z, Hu J, Liang W et al. 2017. Two rice receptor-like kinases maintain male fertility under changing temperatures. Proceedings of the National Academy of Sciences, USA 114: 12327-12332.
Yuan SH, Bai JF, Guo HY, Duan WJ, Liu ZH, Zhang FT, Ma JX, Zhao CP, Zhang LP. 2020. QTL mapping of male sterility-related traits in a photoperiod and temperature-sensitive genic male sterile wheat line BS366. Plant Breeding 139: 498-507.
Yuan SC, Zhang ZG, He HH, Zen HL, Lu KY, Lian JH, Wang BX. 1993. Two photoperiodic-reactions in photoperiod-sensitive genic male-sterile rice. Crop Science 33: 651-660.
Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L et al. 2009. RNA interference of LIN5 in tomato confirms its role in controlling brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology 150: 1204-1218.
Zhang D, Luo X, Zhu L. 2011. Cytological analysis and genetic control of rice anther development. Journal of Genetics and Genomics 38: 379-390.
Zhang D, Yang L. 2014. Specification of tapetum and microsporocyte cells within the anther. Current Opinion in Plant Biology 17: 49-55.
Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, Zhang D. 2010. Carbon Starved Anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22: 672-689.
Zhang H, Xu C, He Y, Zong J, Yang X, Si H, Sun Z, Hu J, Liang W, Zhang D. 2013. Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proceedings of the National Academy of Sciences, USA 110: 76-81.
Zhang H, Zhang J, Wei P, Zhang B, Gou F, Feng Z, Mao Y, Yang L, Zhang H, Xu N et al. 2014. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnology Journal 12: 797-807.
Zhang Y, Liang W, Shi J, Xu J, Zhang D. 2013. MYB56 encoding a R2R3 MYB transcription factor regulates seed size in Arabidopsis thaliana. Journal of Integrative Plant Biology 55: 1166-1178.
Zhou H, Liu Q, Li J, Jiang D, Zhou L, Wu P, Lu S, Li F, Zhu L, Liu Z et al. 2012. Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Research 22: 649-660.
Zhou H, Zhou M, Yang Y, Li J, Zhu L, Jiang D, Dong J, Liu Q, Gu L, Zhou L et al. 2014. RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nature Communications 5: 4884-5884.
Zhou R, Quebedeaux B. 2003. Changes in photosynthesis and carbohydrate metabolism in mature apple leaves in response to whole plant source-sink manipulation. Journal of the American Society for Horticultural Science 128: 113-119.
Zhu X, Liang W, Cui X, Chen M, Yin C, Luo Z, Zhu J, Lucas WJ, Wang Z, Zhang D. 2015. Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein. The Plant Journal 82: 570-581.