三种藓类植物固碳耗水节律调节作用

doi:10.17521/cjpe.2022.0153

植物生态学报 ›› 2023, Vol. 47 ›› Issue (7): 988-997.DOI: 10.17521/cjpe.2022.0153

所属专题：光合作用

三种藓类植物固碳耗水节律调节作用

蒋海港¹, 曾云鸿¹, 唐华欣¹, 刘伟¹, 李杰林¹, 何国华¹, 秦海燕¹, 王丽超¹, 姚银安¹^,^*()

¹西南科技大学生命科学与工程学院, 四川绵阳 621002
²Department of Crop and Forest Sciences, University of Lleida, Lleida, Spain

收稿日期:2022-04-18 接受日期:2022-09-28 出版日期:2023-07-20 发布日期:2023-07-21
通讯作者: *(姚银安, yinanyao@swust.edu.cn; Resco de Dios V, v.rescodedios@gmail.com)
基金资助:
国家高层次人才项目(20zg2102);基金委区域基金重点项目(U20A2079);四川省创新人才项目(2020JDRC0065)

Rhythmic regulation of carbon fixation and water dissipation in three mosses

JIANG Hai-Gang¹, ZENG Yun-Hong¹, TANG Hua-Xin¹, LIU Wei¹, LI Jie-Lin¹, HE Guo-Hua¹, QIN Hai-Yan¹, WANG Li-Chao¹, Victor RESCO de DIOS¹^,²^,^*(), YAO Yin-An¹^,^*()

¹School of Life Science and Engineering, Southwest University of Science and Technology, Mianyang, Sichuan 621002, China
²Department of Crop and Forest Sciences, University of Lleida, Lleida, Spain

Received:2022-04-18 Accepted:2022-09-28 Online:2023-07-20 Published:2023-07-21
Contact: *(Yao YA, yinanyao@swust.edu.cn; Resco de Dios V, v.rescodedios@gmail.com)
Supported by:
The National High-level Talents Project of China(20zg2102);The Regional Fund Key Project of the Foundation Committee of China(U20A2079);The National High-level Talents Project of China(2020JDRC0065)

摘要/Abstract

摘要：

藓类植物作为缺乏维管组织的非等水植物, 其光合作用和耗水量主要受到光照、温度和水分供应状况的影响; 这些环境条件随昼夜交替改变, 是否使得藓类植物形成了类似维管植物的内在昼夜节律调节机制, 目前还所知甚少; 理解其节律响应特点对于藓类植物的保育与利用具有重要意义。该研究对脆枝青藓(Brachythecium thraustum)、大灰藓(Hypnum plumaeforme)和长叶提灯藓(Mnium lycopodioides)进行12 h/12 h的昼夜光周期驯化后进行24 h/0 h的持续光照处理, 分别测定3种藓类在12 h/12 h和24 h/0 h光周期条件下的净光合速率(P_n)和蒸腾速率(T_r), 结果表明: 排除光照和叶-气水汽压差(VPD)等环境影响之后, 3种藓类的这两个指标均观察到明显的节律变化, 节律调节作用能够解释其P_n和T_r日变化的23.4%和30.2%; 且维管植物中少见的T_r节律作用出现在所有受试的藓类植物上; P_n和T_r的节律响应存在明显的种间差异, 该研究中节律性最强的物种为脆枝青藓。以脆枝青藓为例进一步分析其全光照下非结构性碳水化合物(NSC)的节律响应时序转录组, 结果表明: 35.1%的淀粉、糖类合成代谢相关基因的表达具有节律性, 且与NSC含量的昼夜节律变化相关; 脱落酸信号和气孔调节相关基因的表达变化与T_r的节律调节相关; 光合电子传递和暗反应相关蛋白的转录水平变化与光合作用节律保持一致。藓类植物虽然丢失了生物钟核心反馈环CCA1/LHY基因, 但是核心生物钟功能集中于PRRs家族, 通过级联调节使得光合作用生物学过程和保卫细胞水分/离子运输过程等相关基因表达呈现显著的节律性, 最终导致固碳耗水的节律响应高度保守。

关键词: 昼夜节律, 转录组, 光合作用, 蒸腾作用, 气孔, 脆枝青藓, 大灰藓, 长叶提灯藓

Abstract:

Aims As anisohydric plants lacking vascular tissue, mosses are thought to be influenced on their water movement and photosynthesis mainly by the water status and light of the ambient environment. Do the mosses develop an intrinsic circadian regulation mechanism similar to that of vascular plants as these environmental conditions change with day and night alteration? Understanding its rhythmic response characteristics is of great significance for the conservation and utilization of the mosses.

Methods The Brachythecium thraustum, Hypnum plumaeforme and Mnium lycopodioides were trained to 12 h/12 h light-dark (LD) cycles before transfer to 24 h/0 h constant light. We measured the three mosses’ net photosynthetic rate (P_n) and transpiration rate (T_r) on the constant light and last day of the light-dark cycles. Subsequently, non-structural carbon (NSC) content was measured for Brachythecium thraustum. Finally, we sequenced the Brachythecium thraustum transcriptomes in a time series in constant light conditions.

Important findings We found the significant rhythmic changes in the P_n and T_r of the three mosses when excluding environmental influences such as light and vapor pressure difference (VPD), and rhythmic regulation could explain 23.4% and 30.2% of the diurnal changes in P_n and T_r. Moreover, the rhythmic effect of T_r, which is rarely observed in vascular plants, appeared in all the mosses tested, and the rhythmic responses of P_n and T_r were different among species. The species with the strongest rhythm in this study was Brachythecium thraustum, and it was further analyzed for the rhythmic responses of time-series transcriptome and its NSC content under full light. The results showed that 35.1% of starch and carbohydrate biosynthesis-related genes showed rhythmic expression, which was closely related to NSC content change. In addition, the rhythmic regulation of T_r was associated with the transcript changes of abscisic acid signaling and stomatal regulation. Furthermore, the photosynthesis rhythms were associated with transcript changes of photosynthesis-related protein, like photosynthetic electron transport and carbon sequestration proteins. Although the CCA1/LHY genes, the core feedback loop of the circadian clock, have been lost in the mosses, the core circadian clock function concentrates in the PRRs family. The rhythmic response to carbon sequestration and water consumption is highly conserved.

Key words: circadian rhythm, transcriptome, photosynthesis, transpiration, stomata, Brachythecium thraustum, Hypnum plumaeforme, Mnium lycopodioides

蒋海港, 曾云鸿, 唐华欣, 刘伟, 李杰林, 何国华, 秦海燕, 王丽超, 姚银安. 三种藓类植物固碳耗水节律调节作用. 植物生态学报, 2023, 47(7): 988-997. DOI: 10.17521/cjpe.2022.0153

JIANG Hai-Gang, ZENG Yun-Hong, TANG Hua-Xin, LIU Wei, LI Jie-Lin, HE Guo-Hua, QIN Hai-Yan, WANG Li-Chao, Victor RESCO de DIOS, YAO Yin-An. Rhythmic regulation of carbon fixation and water dissipation in three mosses. Chinese Journal of Plant Ecology, 2023, 47(7): 988-997. DOI: 10.17521/cjpe.2022.0153

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0153

https://www.plant-ecology.com/CN/Y2023/V47/I7/988

图/表 3

图1 使用广义相加模型(GAM)拟合脆枝青藓、大灰藓和长叶提灯藓的净光合同化速率(Pn)、蒸腾速率(Tr)、非结构性碳水化合物和核心生物钟基因及节律调控相关基因昼夜节律。A、B中灰色部分对应于15 d正常光周期的最后一个夜晚。横坐标上的黑色和白色分别代表植物自然条件下的夜晚和白天, 灰色部分代表植物自然条件下黑暗但给予光照。C-I中灰色部分表示全光照条件下第二天(LL2d)外界条件下的夜晚。D-I分别为脆枝青藓生物钟调控相关基因的表达量。CDF1, CYCLING DOF FACTOR1; CKB, CASEIN KINASE II BETA CHAIN; CO, Constans; PAP1, PRODUCTION OF ANTHOCYANIN PIGMENT 1; PRR7, PSEUDO RESPONSE REGULATOR 7; PRR9, PSEUDO RESPONSE REGULATOR。

Fig. 1 Circadian rhythms of core circadian clock genes and rhythm regulation-related genes fitted to photosynthetic assimilation rate (Pn), transpiration rate (Tr), and non-structural carbon (NSC) in Brachythecium thraustum、Hypnum plumaeforme and Mnium lycopodioides using generalized additive model (GAM). The gray part in A and B corresponds to the last night of the 15 d normal photoperiod. The black and white parts on the horizontal coordinates represent the night and daytime of the plant under natural conditions, respectively, while the gray part represents the darkness of the plant under natural conditions but given light. The gray part in C-I represents the night under full light conditions on the second day (LL2d) under external conditions. D-I represent expression of clock-regulated genes in the moss Ceratodon purpureus. CDF1, CYCLING DOF FACTOR1; CKB, CASEIN KINASE II BETA CHAIN; CO, Constans; PAP1, PRODUCTION OF ANTHOCYANIN PIGMENT 1; PRR7, PSEUDO RESPONSE REGULATOR 7; PRR9, PSEUDO RESPONSE REGULATOR.

图2 在恒定光照下脆枝青藓相关基因的表达。A, 15个显著的气孔相关节律性基因热图。B, 25个显著的光合相关节律性基因热图。C, 20个显著的非结构性碳水化合物相关节律性基因热图。热图采用了归一化表达量, 范围为-1.5到1.5。

Fig. 2 Expression of significant rhythmic genes related to stomata (A), photosynthesis(B) and non-structural carbohydrates (C) for Brachythecium thraustum under continuous illumination and constant environmental conditions. The heatmap used normalized expression levels, ranging from -1.5 to 1.5.

图3 脆枝青藓相关基因的相关性分析。A, 15个显著的气孔相关节律性基因主成分(PC)分析图。B, 57个显著的碳固定相关节律性基因相关性图, 红色表示正相关, 蓝色表示负相关。C, 159个显著的光合相关节律性基因相关性图。热图采用了归一化表达量, 范围为-1到1。蓝色区域代表高表达量, 而红色区域则代表低表达量。ACA10, Ca2 +-ATP酶10; AHA5, 质膜H+-ATP酶; AHA10, H+-ATP酶10; MTC, PSII反应中心相关的膜内捕光复合物; OST1, 气孔开放因子1; PEX, 光系统II (PSII)外围蛋白质; PIP2;1, 水通道蛋白PIP2-1; Pn, 净光合速率; Tr, 蒸腾速率。

Fig. 3 Correlation analysis of genes related to Brachythecium thraustum. Principal Component (PC) analysis of 15 significant stomatal-related rhythmicity genes (A), 57 significant carbon fixation-related rhythmicity genes correlation plot (B) and 159 significant photosynthesis-related rhythmicity genes correlation plot (C) of Brachythecium thraustum. Red color indicates positive correlation, blue color indicates negative correlation. The heatmap used normalized expression levels, ranging from -1 to 1. In this scheme, blue regions represent high expression levels, while red regions represent low expression levels. ACA10, Ca2+-ATPase 10; AHA5, plasma membrane H+-ATPase 5; AHA10, H+-ATPase 10; MTC, membrane-intrinsic light-harvesting complexes associated with PSII reaction centers; OST1, open stomata 1; PEX, photosystem II (PSII) extrinsic proteins; PIP2;1, aquaporin PIP2-1; Pn, photosynthetic rate; Tr, transpiration rate.

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三种藓类植物固碳耗水节律调节作用

Rhythmic regulation of carbon fixation and water dissipation in three mosses

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