
Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen
Received date: 2024-07-02
Accepted date: 2024-10-10
Online published: 2024-10-22
Honglian type-cytoplasmic male sterility (HL-CMS) is caused by the inter-communication between the nucleus and mitochondria. However, the mechanisms by which sterility genes regulate metabolic alterations and changes in mitochondrial morphology in the pollen of HL-CMS remain unclear. In this study, we compared the morphological differences between the pollen of the male sterile line YA and the near-isogenic line NIL-Rf6 using hematoxylin-eosin staining and 4ʹ,6-diamidino-2-phenylindole (DAPI) staining. HL-CMS is characterized by gametophytic sterility, where the aborted pollen grains are empty, and the tapetal layer remains intact. Transmission electron microscopy was employed to observe mitochondrial morphological changes at the microspore stage, revealing significant mitochondrial alterations, characterized by the formation of 'large spherical mitochondria', occurred at the binucleate stage in the YA line. Additionally, metabolomics analysis revealed decreased levels of metabolites associated with the carbohydrate and flavonoid pathways. Notably, the decrease in flavonoids was found to contribute to an elevation in reactive oxygen species (ROS) levels. Therefore, we propose a model in which rice fertility is modulated by the levels of pollen carbohydrates and flavonoid metabolites, with impaired mitochondrial energy production and reduced flavonoid biosynthesis as the main causes of ROS accumulation and pollen abortion in rice.
Wang Mingyue, Zhao Weibo, Feng Xiaoya, Chen Yi, Li Junhao, Fu Jinmei, Yan Yingchun, Chu Zhaohui, Huang Wenchao . Disruption of Energy Metabolism and Reactive Oxygen Species Homeostasis in Honglian Type-Cytoplasmic Male Sterility (HL-CMS) Rice Pollen[J]. Rice Science, 2025 , 32(1) : 81 -93 . DOI: 10.1016/j.rsci.2024.10.003
| [1] | Annesley S J, Fisher P R. 2019. Mitochondria in health and disease. Cells, 8(7): 680. |
| [2] | Barrera-Paez J D, Moraes C T. 2022. Mitochondrial genome engineering coming-of-age. Trends Genet, 38(8): 869-880. |
| [3] | Bian X H, Li W, Niu C F, et al. 2020. A class B heat shock factor selected for during soybean domestication contributes to salt tolerance by promoting flavonoid biosynthesis. New Phytol, 225(1): 268-283. |
| [4] | Charlesworth D. 2017. Origins of rice cytoplasmic male sterility genes. Cell Res, 27(1): 3-4. |
| [5] | Chase C D. 2007. Cytoplasmic male sterility: A window to the world of plant mitochondrial-nuclear interactions. Trends Genet, 23(2): 81-90. |
| [6] | Che R H, Hu B, Wang W, et al. 2022. POLLEN STERILITY, a novel suppressor of cell division, is required for timely tapetal programmed cell death in rice. Sci China Life Sci, 65(6): 1235-1247. |
| [7] | Ding X L, Wang X, Li Q, et al. 2019. Metabolomics studies on cytoplasmic male sterility during flower bud development in soybean. Int J Mol Sci, 20(12): 2869. |
| [8] | Ding X L, Guo J F, Lv M L, et al. 2023. The miR156b-GmSPL2b module mediates male fertility regulation of cytoplasmic male sterility-based restorer line under high-temperature stress in soybean. Plant Biotechnol J, 21(8): 1542-1559. |
| [9] | Farooq M A, Niazi A K, Akhtar J, et al. 2019. Acquiring control: The evolution of ROS-induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol Biochem, 141: 353-369. |
| [10] | Feng J H, Lu Y G, Liu X D, et al. 2001. Pollen development and its stages in rice (Oryza sativa L.). Chin J Rice Sci, 15(1): 21-28. (in Chinese with English abstract) |
| [11] | Fujii S, Toriyama K. 2009. Suppressed expression of RETROGRADE- REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. Proc Natl Acad Sci USA, 106(23): 9513-9518. |
| [12] | Gass N, Glagotskaia T, Mellema S, et al. 2005. Pyruvate decarboxylase provides growing pollen tubes with a competitive advantage in Petunia. Plant Cell, 17(8): 2355-2368. |
| [13] | Hanson A D, Henry C S, Fiehn O, et al. 2016. Metabolite damage and metabolite damage control in plants. Annu Rev Plant Biol, 67: 131-152. |
| [14] | Hao T S, Yu J L, Wu Z D, et al. 2023. Hypoxia-reprogramed megamitochondrion contacts and engulfs lysosome to mediate mitochondrial self-digestion. Nat Commun, 14(1): 4105. |
| [15] | Huang W C, Hu J, Yu C C, et al. 2012. Two non-allelic nuclear genes restore fertility in a gametophytic pattern and enhance abiotic stress tolerance in the hybrid rice plant. Theor Appl Genet, 124(5): 799-807. |
| [16] | Huang W C, Yu C C, Hu J, et al. 2015. Pentatricopeptide-repeat family protein RF6 functions with hexokinase 6 to rescue rice cytoplasmic male sterility. Petroc Natl Acad Sci USA, 112(48): 14984-14989. |
| [17] | Kazama T, Itabashi E, Fujii S, et al. 2016. Mitochondrial ORF79 levels determine pollen abortion in cytoplasmic male sterile rice. Plant J, 85(6): 707-716. |
| [18] | Li S Q, Wan C X, Kong J, et al. 2004. Programmed cell death during microgenesis in a Honglian CMS line of rice is correlated with oxidative stress in mitochondria. Funct Plant Biol, 31(4): 369-376. |
| [19] | Muhlemann J K, Younts T L B, Muday G K. 2018. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc Natl Acad Sci USA, 115(47): E11188-E11197. |
| [20] | Raimundo N. 2014. Mitochondrial pathology: Stress signals from the energy factory. Trends Mol Med, 20(5): 282-292. |
| [21] | Rejón J D, Delalande F, Schaeffer-Reiss C, et al. 2016. The pollen coat proteome: At the cutting edge of plant reproduction. Proteomes, 4(1): 5. |
| [22] | Santiago J P, Sharkey T D. 2019. Pollen development at high temperature and role of carbon and nitrogen metabolites. Plant Cell Environ, 42(10): 2759-2775. |
| [23] | Tang H L, Song Y L, Guo J L, et al. 2018. Physiological and metabolome changes during anther development in wheat (Triticum aestivum L.). Plant Physiol Biochem, 132: 18-32. |
| [24] | Tang M Q, Li Z Q, Luo D J, et al. 2021. A comprehensive integrated transcriptome and metabolome analyses to reveal key genes and essential metabolic pathways involved in CMS in kenaf. Plant Cell Rep, 40(1): 223-236. |
| [25] | Wang K, Gao F, Ji Y X, et al. 2013. ORFH79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice. New Phytol, 198(2): 408-418. |
| [26] | Wang L X, Ying Lam L P, Lui A C W, et al. 2020. Flavonoids are indispensable for complete male fertility in rice. J Exp Bot, 71(16): 4715-4728. |
| [27] | Wu H M, Xie D J, Jia P F, et al. 2023. Homeostasis of flavonoids and triterpenoids most likely modulates starch metabolism for pollen tube penetration in rice. Plant Biotechnol J, 21(9): 1757-1772. |
| [28] | Xiao S L, Song W, Xing J F, et al. 2023. ORF355 confers enhanced salinity stress adaptability to S-type cytoplasmic male sterility maize by modulating the mitochondrial metabolic homeostasis. J Integr Plant Biol, 65(3): 656-673. |
| [29] | Yamasaki H, Heshiki R, Ikehara N. 1995. Leaf-goldenning induced by high light in Ficus microcarpa L. f., a tropical fig. J Plant Res, 108(2): 171-180. |
| [30] | Yan J J, Tian H, Wang S Z, et al. 2014. Pollen developmental defects in ZD-CMS rice line explored by cytological, molecular and proteomic approaches. J Proteomics, 108: 110-123. |
| [31] | Yu L, McPhee C K, Zheng L X, et al. 2010. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature, 465: 942-946. |
| [32] | Yu X W, Zhao Z G, Zheng X M, et al. 2018. A selfish genetic element confers non-Mendelian inheritance in rice. Science, 360: 1130-1132. |
| [33] | Zang R, Shahzad K, Zhang X X, et al. 2023. Dose effects of restorer gene modulate pollen fertility in cotton CMS-D2 restorer lines via auxin signaling and flavonoid biosynthesis. Plant Cell Rep, 42(11): 1705-1719. |
| [34] | Zhang D B, Luo X, Zhu L. 2011. Cytological analysis and genetic control of rice anther development. J Genet Genomics, 38(9): 379-390. |
| [35] | Zhao W, Hou Q C, Qi Y C, et al. 2023. Structural and molecular basis of pollen germination. Plant Physiol Biochem, 203: 108042. |
| [36] | Zheng X M, Wei F, Cheng C, et al. 2024. A historical review of hybrid rice breeding. J Integr Plant Biol, 66(3): 532-545. |
| [37] | Zu X F, Luo L L, Wang Z, et al. 2023. A mitochondrial pentatricopeptide repeat protein enhances cold tolerance by modulating mitochondrial superoxide in rice. Nat Commun, 14(1): 6789. |
/
| 〈 |
|
〉 |