生理和通路分析结合揭示黑穗病菌对糜子光合作用的影响

doi:10.1016/j.jia.2023.12.027

摘要/Abstract

摘要：

光合作用是作物生长的基础，对逆境胁迫敏感。黑穗病(Sporisorium destruens)是糜子生产的主要病害。本研究评估了S. destruens侵染对抗病糜子和感病糜子光合作用的影响。接种后，两个品种叶片的叶绿素含量，气体交换参数和叶绿素荧光参数均下降；发病植株叶片超微结构显示叶绿体、线粒体结构异常，并产生许多液泡。抽穗期对各处理的旗叶进行RNA-Seq测序，除抗病和感病糜子外，将发病植株顶部由花序发育而来的病叶作为S2。分析结果表明接种后与光合作用有关的通路诱导了大量的差异表达基因(DEGs)，其中感病糜子NF诱导的DEGs数量比抗病糜子BM多，S2诱导的DEGs数量多于感病糜子NF。在这些DEGs中，感病品种诱导的下调DEGs数量大于上调数量， S2诱导的DEGs中上调数量大于下调数量。这些结果表明S. destruens侵染影响了糜子的正常的光合特性。了解S. destruens、光合作用和糜子之间的互作机制是预防黑穗病的发生及增强其抗性的有效措施。

Abstract:

Photosynthesis is the basis of crop growth and is sensitive to stress. Smut (Sporisorium destruens) is the primary disease in the production of broomcorn millet (Panicum miliaceum L.). This study evaluated the effects of infection with S. destruens on the photosynthesis of the resistant cultivar (BM) and susceptible cultivar (NF). After inoculation, there was a decrease in the chlorophyll content, gas exchange parameters, and chlorophyll fluorescence of the two cultivars. Observation of the ultrastructure of diseased leaves showed that the chloroplasts and mitochondria had abnormal morphology, and some vacuoles appeared. RNA-seq was performed on the flag leaves after inoculation. In addition to the resistant and susceptible cultivars, the diseased leaves developed from inflorescences were defined as S2. The analysis showed that the pathways related to photosynthesis stimulated some differentially expressed genes (DEGs) after infection with S. destruens. More DEGs were induced in the susceptible broomcorn millet NF than in the resistant broomcorn millet BM, and most of those genes were downregulated. The number of DEGs induced by S2 was greater than that in susceptible cultivar NF, and most of them were upregulated. These results indicate that infection with S. destruens affects the normal photosynthetic performance of broomcorn millet. Understanding the mechanism between S. destruens, photosynthesis, and broomcorn millet is an effective measure to prevent the occurrence of smut and enhance its resistance.

Key words: broomcorn millet , smut , Sporisorium destruens , photosynthesis

Fei Jin, Lei Xu, Zhihu Lü, Yuchuan Zhang, Qinghua Yang, Qingfang Han, Baili Feng. 生理和通路分析结合揭示黑穗病菌对糜子光合作用的影响[J]. Journal of Integrative Agriculture, 2025, 24(3): 1065-1079.

Fei Jin, Lei Xu, Zhihu Lü, Yuchuan Zhang, Qinghua Yang, Qingfang Han, Baili Feng. Combined physiological and pathway analysis revealed the effect of Sporisorium destruens on photosynthesis in broomcorn millet (Panicum miliaceum L.) [J]. Journal of Integrative Agriculture, 2025, 24(3): 1065-1079.

参考文献

Berger S, Sinha A K, Roitsch T. 2007. Plant physiology meets phytopathology: Plant primary metabolism and plant–pathogen interactions. Journal of Experimental Botany, 58, 4019–4026.

Dekker J P, Boekema E J. 2005. Supramolecular organization of thylakoid membrane proteins in green plants. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1706, 12–39.

Doehlemann G, Wahl R, Horst R J, Voll L M, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, Kämper J. 2008a. Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant Journal, 56, 181–195.

Doehlemann G, Wahl R, Vranes M, de Vries R P, Kämper J, Kahmann R. 2008b. Establishment of compatibility in the Ustilago maydis/maize pathosystem. Journal of Plant Physiology, 165, 29–40.

Erickson E, Wakao S, Niyogi K K. 2015. Light stress and photoprotection in Chlamydomonas reinhardtii. Plant Journal, 82, 449–465.

Fernie A R, Bachem C W B, Helariutta Y, Neuhaus H E, Prat S, Ruan Y L, Stitt M, Sweetlove L J, Tegeder M, Wahl V, Sonnewald S, Sonnewald U. 2020. Synchronization of developmental, molecular and metabolic aspects of source–sink interactions. Nature Plants, 6, 55–66.

Gabara B, Kuźniak E, Skłodowska M, Surówka E, Miszalski Z. 2012. Ultrastructural and metabolic modifications at the plant–pathogen interface in Mesembryanthemum crystallinum leaves infected by Botrytis cinerea. Environmental and Experimental Botany, 77, 33–43.

Ghareeb H, Becker A, Iven T, Feussner I, Schirawski J. 2011. Sporisorium reilianum infection changes inflorescence and branching architectures of maize. Plant Physiologgy, 156, 2037–2052.

Goldschmidt-Clermont M, Bassi R. 2015. Sharing light between two photosystems: Mechanism of state transitions. Current Opinion in Plant Biology, 25, 71–78.

Gong X, Dang K, Liu L, Zhao G, Lv S, Tian L, Jin F, Feng Y, Zhao Y, Feng B. 2021. Intercropping combined with nitrogen input promotes proso millet (Panicum miliaceum L.) growth and resource use efficiency to increase grain yield on the Loess plateau of China. Agricultural Water Management, 243, 106434.

De Groote H, Munyua B G. Palmas S, Suresh L M, Bruce A Y, Kimenju S. 2021. Using panel community surveys to track the impact of crop pests over time and space - The case of maize lethal necrosis (MLN) disease in Kenya from 2013 to 2018. Plant Disease, 105, 1259–1271.

Habiyaremye C, Matanguihan J B, Guedes J D, Ganjyal G M, Whiteman M R, Kidwell K K, Murphy K M. 2017. Proso millet (Panicum miliaceum L.) and its potential for cultivation in the Pacific Northwest, U.S.: A review. Fronters in Plant Science, 7, 1961.

Heinig U, Gutensohn M, Dudareva N, Aharoni A. 2013. The challenges of cellular compartmentalization in plant metabolic engineering. Current Opinion in Biotechnology, 24, 239–246.

Horst R J, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, Kahmann R, Kämper J, Sonnewald U, Voll L M. 2010. Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiology, 152, 293–308.

Horst R J, Engelsdorf T, Sonnewald U, Voll L M. 2008. Infection of maize leaves with Ustilago maydis prevents establishment of C4 photosynthesis. Journal of Plant Physiology, 165, 19–28.

Jin F, Liu J, Wu E, Yang P, Gao J, Gao X, Feng B. 2021. Leaf transcriptome analysis of broomcorn millet uncovers key genes and pathways in response to Sporisorium destruens. International Journal of Molecular Sciences, 22, 9542.

Kahmann R, Kämper J. 2004. Ustilago maydis: How its biology relates to pathogenic development. New Phytologist, 164, 31–42.

Leister D. 2019. Genetic engineering, synthetic biology and the light reactions of photosynthesis. Plant Physiology, 179, 778–793.

Liu C, Yuan Y, Liu J, Wang H, Ma Q, Zhou Y, Liu C, Gong X, Feng B. 2022 Comparative transcriptome and physiological analysis unravel proso millet (Panicum miliaceum L.) source leaf adaptation to nitrogen deficiency with high nitrogen use efficiency. Environmental and Experimental Botany, 199, 104891.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.

Ludewig F, Sonnewald U. 2016. Demand for food as driver for plant sink development. Journal of Plant Physiology, 203, 110–115.

Maejima K, Iwai R, Himeno M, Komatsu K, Kitazawa Y, Fujita N, Ishikawa K, Fukuoka M, Minato N, Yamaji Y, Oshima K, Namba S. 2014. Recognition of floral homeotic MADS domain transcription factors by a phytoplasmal effector, phyllogen, induces phyllody. Plant Journal, 78, 541–554.

Makino A, Suzuki Y, Ishiyama K. 2022. Enhancing photosynthesis and yield in rice with improved N use efficiency. Plant Science, 325, 111475.

Masuda T, Fusada N, Oosawa N, Takamatsu K, Yamamoto Y Y, Ohto M, Nakamura K, Goto K, Shibata D, Shirano Y, Hayashi H, Kato T, Tabata S, Shimada H, Ohta H, Takamiya K. 2003. Functional analysis of isoforms of NADPH: Protochlorophyllide oxidoreductase (POR) in Arabidopsis thaliana. Plant and Cell Physiology, 44, 963–974.

Matheussen A M, Morgan P W, Frederiksen R A. 1991. Implication of gibberellins in head smut (Sporisorium reilianum) of Sorghum bicolor. Plant Physiology, 96, 537–544.

Müller A H, Sawicki A, Zhou S, Tabrizi S T, Luo M, Hansson M, Willows R D. 2014. Inducing the oxidative stress response in Escherichia coli improves the quality of a recombinant protein: Magnesium chelatase ChlH. Protein Expression and Purification, 101, 61–67.

Nagata N, Tanaka R, Satoh S, Tanaka A. 2005. Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell, 17, 233–240.

Negi J, Munemasa S, Song B, Tadakuma R, Fujita M, Azoulay-Shemer T. 2018. Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells. Proceedings of the National Academy of Sciences of the United States of America, 115, 9038–9043.

Nelson N, Yocum C F. 2006. Structure and function of photosystems I and II. Annual Review of Plant Biology, 57, 521–565.

Pérez-Bueno M L, Pineda M, Barón M. 2019. Phenotyping plant responses to biotic stress by chlorophyll fluorescence imaging. Fronters in Plant Science, 10, 1135.

Pruzinská A, Anders I, Aubry S, Schenk N, Tapernoux-Lüthi E, Müller T, Kräutler B, Hörtensteiner S. 2007. In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell, 19, 369–387.

Qiu J, Meng S, Deng Y, Huang S, Kou Y. 2019. Ustilaginoidea virens: A fungus infects rice flower and threats world rice production. Rice Science, 26, 199–206.

Rajput S G, Santra D K, Schnable J. 2016. Mapping QTLs for morpho-agronomic traits in proso millet (Panicum miliaceum L.). Molecular Breeding, 36, 1–18.

Raza M M, Bebber D P. 2022. Climate change and plant pathogens. Current Opinion in Microbiology, 70, 102233.

Ruan X, Ma L, Zhang Y, Wang Q, Gao X. 2021. Dissection of the complex transcription and metabolism regulation networks associated with maize resistance to Ustilago maydis. Genes, 12, 1789.

Sakuraba Y, Rahman M L, Cho S H, Kim Y S, Koh H J, Yoo S C, Paek N C. 2013. The rice faded green leaf locus encodes protochlorophyllide oxidoreductase B and is essential for chlorophyll synthesis under high light conditions. Plant Journal, 74, 122–133.

Santiago R, Alarcón B, de Armas R, Vicente C, Legaz M E. 2012. Changes in cinnamyl alcohol dehydrogenase activities from sugarcane cultivars inoculated with Sporisorium scitamineum sporidia. Physiologia Plantarum, 145, 245–259.

Sawicki A, Zhou S, Kwiatkowski K, Luo M, Willows R D. 2017. 1-N-histidine phosphorylation of ChlD by the AAA+ ChLI2 stimulates magnesium chelatase activity in chlorophyll synthesis. Biochemical Journal, 474, 2095–2105.

Schierhorn F, Hofmann M, Gagalyuk T, Ostapchuk I, Müller D. 2021. Machine learning reveals complex effects of climatic means and weather extremes on wheat yields during different plant developmental stages. Climatic Change, 169, 1–19.

Sonnewald U, Fernie A R. 2018 Next-generation strategies for understanding and influencing source–sink relations in crop plants. Current Opinion in Plant Biology, 43, 63–70.

Tanaka R, Tanaka A. 2007. Tetrapyrrole biosynthesis in higher plants. Annual Review of Plant Biology, 58, 321–346.

Tiku V, Tan M W, Dikic I. 2020. Mitochondrial functions in infection and immunity. Trends in Cell Biollgy, 30, 263–275.

Townsend A J, Ware M A, Ruban A V. 2018. Dynamic interplay between photodamage and photoprotection in photosystem II. Plant, Cell & Environment, 1, 1098–1112.

Turgeon R. 1989. The sink–source transition in leaves. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 119–138.

Villajuana-Bonequi M, Matei A, Ernst C, Hallab A, Usadel B, Doehlemann G. 2019. Cell type specific transcriptional reprogramming of maize leaves during Ustilago maydis induced tumor formation. Scientific Reports, 9, 1–15.

Wang P, Grimm B. 2021. Connecting chlorophyll metabolism with accumulation of the photosynthetic apparatus. Trends in Plant Science, 26, 484–495.

Wobbe L, Bassi R, Kruse O. 2016. Multi-level light capture control in plants and green algae. Trends in Plant Science, 21, 55–68.

Woodson J D. 2022. Control of chloroplast degradation and cell death in response to stress. Trends in Biochemical Sciences, 47, 851–864.

Xiao L, Wang S. 2005. Plant Physiology Experiment Technology. China Agrculture Press, Beijing. pp. 25–28. (in Chinese)

Yuan Y, Liu L, Gao Y, Yang Q, Dong K. Liu T. Feng B. 2022. Comparative analysis of drought-responsive physiological and transcriptome in broomcorn millet (Panicum miliaceum L.) genotypes with contrasting drought tolerance. Industrial Crops and Products, 177, 114498.

Yuan Y H, Li J, Ma H C, Yang Q H, Liu C J, Feng B L. 2021. Salt-tolerant broomcorn millet (Panicum miliaceum L.) resists salt stress via modulation of cell wall biosynthesis and Na+ balance. Land Degradation & Development, 32, 518–532.

Zeeman S C, Smith S M, Smith A M. 2007. The diurnal metabolism of leaf starch. Biochemical Journal, 401, 13–28.

Zhang J, He C, Chen L, Gao S. 2018. Improving food security in China by taking advantage of marginal and degraded lands. Journal of Clean Production, 171, 1020–1030.

Zhang Q Q, Zhong T, E L Z, Xu M L, Dai W X, Sun S C, Ye J R. 2021. GT factor ZmGT-3b is associated with regulation of photosynthesis and defense response to Fusarium graminearum infection in maize seedling. Frontiers in Plant Science, 12, 724133.

Zhou Y, Qu Y, Zhu M, Liu J, Wang Y, Song H, Feng B. 2016. Genetic diversity and virulence variation of Sporisorium destruens isolates and evaluation of broomcorn millet for resistance to head smut. Euphytica, 211, 59–70.

Zou C, Li L, Miki D, Li D, Tang Q, Xiao L, Rajput S, Deng P, Peng L, Jia W, Huang R, Zhang M, Sun Y, Hu J, Fu X, Schnable P S, Chang Y, Li F, Zhang H, Feng B, et al. 2019. The genome of broomcorn millet. Nature Communication, 10, 436.

Zou K, Li Y, Zhang W, Jia Y, Wang Y, Ma Y, Lv X, Xuan Y, Du W. 2022. Early infection response of fungal biotroph Ustilago maydis in maize. Frontiers in Plant Science, 13, 970897.

Zuo W, Ökmen B, Depotter J R L, Ebert M K, Redkar A, Misas Villamil J, Doehlemann G. 2019. Molecular interactions between smut fungi and their host plants. Annual Review of Phytopathology, 57, 411–430.