异源表达异子蓬SaPEPC2基因提高烟草抗旱性和光合特性(长英文摘要）

doi:10.11983/CBB23145

植物学报 ›› 2024, Vol. 59 ›› Issue (4): 585-599.DOI: 10.11983/CBB23145

异源表达异子蓬SaPEPC2基因提高烟草抗旱性和光合特性(长英文摘要）

廖星鑫^,^†, 牛祎^,^†, 多兴武, 阿克也得力·居玛哈孜, 买热哈巴·阿不都克尤木, 热孜瓦尼姑丽·胡甫尔, 兰海燕, 曹婧^*()

新疆大学生命科学与技术学院, 新疆生物资源基因工程重点实验室, 生物学国家级实验教学示范中心, 乌鲁木齐 830017

收稿日期:2023-10-29 接受日期:2024-05-27 出版日期:2024-07-10 发布日期:2024-07-10
通讯作者: 曹婧
作者简介:第一联系人：^† 共同第一作者
基金资助:
新疆维吾尔自治区自然科学基金(2022D01C95);国家自然科学基金(32360066);国家级大学生创新训练计划(202210755069)

Heterologous Expression of Suaeda aralocaspica SaPEPC2 Gene Improves Drought Resistance and Photosynthesis in Transgenic Tobacco

Xingxin Liao^,^†, Yi Niu^,^†, Xingwu Duo, Akeyedeli Jumahazi, Marhaba Abdukuyum, Rizwangul Hufur, Haiyan Lan, Jing Cao^*()

National Demonstration Center for Experimental Biology Education, Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Sciences and Technology, Xinjiang University, Urumqi 830017, China

Received:2023-10-29 Accepted:2024-05-27 Online:2024-07-10 Published:2024-07-10
Contact: Jing Cao
About author:First author contact:^† These authors contributed equally to this paper

摘要/Abstract

摘要： 磷酸烯醇式丙酮酸羧化酶(PEPC)是C₄光合关键酶, 有助于植物在非生物胁迫下抵御逆境。异子蓬(Suaeda aralocaspica)是一种无须Kranz结构即可在单细胞中高效执行C₄光合作用的荒漠盐生植物, 在C₃作物遗传改良方面具有天然优势。以转异子蓬SaPEPC2基因烟草(Nicotiana tabacum)为材料, 探讨了其抗旱功能和光合性能。结果表明, 过表达SaPEPC2提高了烟草叶片持水能力, 可保持叶绿素稳定; 积累更多的渗透调节物质, 增强了抗氧化酶活性, 进而降低了植株体内的活性氧水平, 减轻膜损伤程度; 同时还增强了烟草抗旱相关基因和内源光合基因的表达, 提高了PEPC活性和净光合速率, 可能是促进了烟草体内的“类C₄微循环”途径所致。研究结果为进一步利用异子蓬单细胞C₄途径PEPC基因培育高光效抗逆农作物品种奠定了基础。

关键词: 单细胞C₄植物, 异子蓬, PEPC, 抗旱性, 光合作用

Abstract: INTRODUCTION: Phosphoenolpyruvate carboxylase (PEPC) is a key enzyme for C₄ photosynthesis that help plants to resist adversity under abiotic stress. Suaeda aralocaspica, an annual halophyte, has gradually developed a single-cell C₄ photosynthetic pathway by compartmentalizing a chlorenchyma cell into distal and proximal ends to delineate and form the four-carbon (C₄) and three-carbon (C₃) cycles through long term of evolution. This unique biochemical compartmentation pattern holds promise for introducing “C₄-like microcirculation” into C₃plants without establishing Kranz anatomy.

RATIONALE: The PEPC gene act as an essential component of C₄ photosynthesis, but few studies have reported on the PEPC gene in single cell C₄-pathway species. To reveal the impact of the SaPEPC2 gene from S. aralocaspica on the photosynthetic performance and drought resistance of C₃ plants, we evaluated the drought resistance function and photosynthetic performance of transgenic tobacco (Nicotiana tabacum) overexpressing the SaPEPC2 gene driven by its own promoter (Pro_SaPEPC2::SaPEPC2) through physiological measurements and gene expression analysis methods.

RESULTS: Our findings demonstrated that overexpressing the SaPEPC2 gene in tobacco improved leaf water retention, maintained chlorophyll stability, promoted the accumulation of osmotic adjustment substance, enhanced antioxidant enzyme activities, reduced ROS levels, mitigated the extent of membrane damage, upregulated the expression of drought-related and endogenous photosynthesis genes, and increased PEPC enzyme activity and net photosynthetic rate.

CONCLUSION: In conclusion, overexpressing the SaPEPC2 gene likely facilitates the formation of a “C₄-like microcircula-

tion” pathway in tobacco. These results may provide the theoretical foundation for the potential utilization of the single-cell C₄ pathway PEPC genes from S. aralocaspica to breed high light-efficiency and stress-resistant crop varieties.

Overexpression of SaPEPC2 in tobacco results in stronger drought resistance and higher photosynthesis efficiency compared to non-transgenic plants.

Key words: single-cell C₄ plant, Suaeda aralocaspica, PEPC, drought resistance, photosynthesis

廖星鑫, 牛祎, 多兴武, 阿克也得力·居玛哈孜, 买热哈巴·阿不都克尤木, 热孜瓦尼姑丽·胡甫尔, 兰海燕, 曹婧. 异源表达异子蓬SaPEPC2基因提高烟草抗旱性和光合特性(长英文摘要）. 植物学报, 2024, 59(4): 585-599.

Xingxin Liao, Yi Niu, Xingwu Duo, Akeyedeli Jumahazi, Marhaba Abdukuyum, Rizwangul Hufur, Haiyan Lan, Jing Cao. Heterologous Expression of Suaeda aralocaspica SaPEPC2 Gene Improves Drought Resistance and Photosynthesis in Transgenic Tobacco. Chinese Bulletin of Botany, 2024, 59(4): 585-599.

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图/表 8

图1 SaPEPC2转基因烟草基因组DNA PCR (A)、RT-PCR (B)、qRT-PCR (C)和Western blot (D)鉴定 M: DL2000分子量标准; -: 阴性对照; +: 阳性对照; NT: NC89非转基因烟草; 1-12: 转基因株系。*** P<0.001; **** P<0.0001 (Student’s t test)

Figure 1 Identification of SaPEPC2 in transgenic tobacco by genomic DNA PCR (A), RT-PCR (B), qRT-PCR (C) and Western blot (D) M: DL2000 marker; -: Negative control; +: Positive control; NT: NC89 non-transgenic tobacco; 1-12: Transgenic lines. *** P<0.001; **** P<0.0001 (Student’s t test)

图2 自然干旱条件下过表达SaPEPC2转基因烟草表型(A)、叶片存活数(B)、失水率(C)和相对含水量(D) 不同小写字母表示不同株系在P<0.05水平差异显著。* P<0.05; ** P<0.01 (Student’s t检验)。NT: 非转基因。OE5、OE7、OE13为不同转基因株系。Bars=2 cm

Figure 2 Phenotype (A), leaf survival number (B), water loss rate (C) and relative water content (D) in SaPEPC2 overexpression transgenic tobacco lines under natural drought conditions Different lowercase letters indicate significant differences among different lines at P<0.05 level. * P<0.05; ** P<0.01 (Student’s t test). NT: Non-transgenic. OE5, OE7 and OE13 are different transgenic individuals. Bars=2 cm

图3 干旱胁迫下过表达SaPEPC2转基因烟草的生理指标 (A) 丙二醛(MDA)含量; (B) H2O2含量; (C) O2-.含量; (D) 脯氨酸含量; (E) 可溶性糖(SS)含量; (F) 甜菜碱含量; (G) 超氧化物歧化酶(SOD)活性; (H) 过氧化物酶(POD)活性; (I) 过氧化氢酶(CAT)活性。*、**和***分别表示转基因植株与非转基因(NT)植株在0.05、0.01和0.001水平存在显著差异(Student’s t检验)。OE5、OE7和OE13同图2。

Figure 3 Physiological indicators in SaPEPC2 overexpression transgenic tobacco lines under drought stress (A) Malondialdehyde (MDA) content; (B) H2O2 content; (C) O2-. content; (D) Proline content; (E) Soluble sugar (SS) content; (F) Betaine content; (G) Superoxide dismutase (SOD) activity; (H) Peroxidase (POD) activity; (I) Catalase (CAT) activity. *, **, and *** indicate significant differences existing between the transgenic line and non-transgenic (NT) plant at 0.05, 0.01, and 0.001 levels, respectively (Student’s t test). OE5, OE7 and OE13 are the same as shownin Figure 2.

图4 干旱胁迫下过表达SaPEPC2转基因烟草干旱胁迫响应基因的表达模式 (A) NtP5CS (编码吡咯烷-5-羧酸合酶); (B) NtERD (脱水诱导早期应答基因); (C) NtDREB1 (编码脱水响应元件结合蛋白)。*、**、***和****分别表示转基因植株与非转基因(NT)植株在0.05、0.01、0.001和0.0001水平存在显著差异(Student’s t检验)。

Figure 4 Expression patterns of drought stress-responsible genes in SaPEPC2 overexpression transgenic tobacco lines under drought stress (A) NtP5CS (encoding pyrroline-5-carboxylate synthase); (B) NtERD (early responsive to dehydration); (C) NtDREB1 (encoding dehydration responsive element binding protein). *, **, ***, and **** indicate significant differences existing between the transgenic line and non-transgenic (NT) plant at 0.05, 0.01, 0.001, and 0.0001 levels, respectively (Student’s t test).

图5 干旱胁迫下过表达SaPEPC2转基因烟草叶绿素含量和光合酶活性 (A) 叶绿素a含量; (B) 叶绿素b含量; (C) 总叶绿素含量; (D) 磷酸烯醇式丙酮酸羧化酶(PEPC)活性; (E) Rubisco酶活性。*、**、***和****分别表示转基因植株与非转基因(NT)植株在0.05、0.01、0.001和0.0001水平存在显著差异(Student’s t检验)。

Figure 5 Chlorophyll content and photosynthetic enzyme activity in SaPEPC2 overexpression transgenic tobacco lines under drought stress (A) Chlorophyll a content; (B) Chlorophyll b content; (C) Total chlorophyll content; (D) Phosphoenolpyruvate carboxylase (PEPC) activity; (E) Rubisco activity. *, **, ***, and **** indicate significant differences existing between the transgenic line and non- transgenic (NT) plant at 0.05, 0.01, 0.001, and 0.0001 levels, respectively (Student’s t test).

图6 干旱胁迫下过表达SaPEPC2转基因烟草内源光合基因的表达模式 (A) NtPEPC; (B) NtCA (编码磷酸酐酶); (C) NtFBP (编码果糖-1,6-二磷酸酶); (D) NtTPT (编码磷酸丙糖转运器)。*、**、***和****分别表示转基因植株与非转基因(NT)植株在0.05、0.01、0.001和0.0001水平存在显著差异(Student’s t检验)。

Figure 6 Expression patterns of endogenous photosynthetic genes in SaPEPC2 overexpression transgenic tobacco lines under drought stress (A) NtPEPC; (B) NtCA (encoding carbonic anhydrase); (C) NtFBP (encoding fructose-1,6-bisphosphatase); (D) NtTPT (encoding triose phosphate translocator). *, **, ***, and **** indicate significant differences existing between the transgenic line and non-transgenic (NT) plant at 0.05, 0.01, 0.001, and 0.0001 levels, respectively (Student’s t test).

图7 过表达SaPEPC2转基因烟草光合指标 (A) 净光合速率(Pn); (B) 气孔导度(Gs); (C) 蒸腾速率(Tr); (D) 胞间CO2浓度(Ci)。L: 大(7-8叶期)植株; M: 中(6-7叶期)植株; S: 小(5-6叶期)植株。*、**、***和****分别表示转基因植株与非转基因(NT)植株在0.05、0.01、0.001和0.0001水平存在显著差异(Student’s t检验)。

Figure 7 Photosynthetic indicators in SaPEPC2 overexpression transgenic tobacco lines (A) Net photosynthetic rate (Pn); (B) Stomatal conductance (Gs); (C) Transpiration rate (Tr); (D) Intercellular CO2 concentration (Ci). L: Large (7-8 leaf stage) plants; M: Medium (6-7 leaf stage) plants; S: Small (5-6 leaf stage) plants. *, **, ***, and **** indicate significant differences existing between the transgenic line and non-transgenic (NT) plant at 0.05, 0.01, 0.001, and 0.0001 levels, respectively (Student’s t test).

图8 过表达SaPEPC2转基因烟草生长指标 (A) 株高; (B) 茎粗; (C) 叶片数; (D) 叶长; (E) 叶宽; (F) 叶面积; (G) 生物量。L、M和S同图7。*、**和***分别表示转基因株系与非转基因(NT)植株在0.05、0.01和0.001水平存在显著差异(Student’s t检验)。

Figure 8 Growth indexes of SaPEPC2 overexpression transgenic tobacco lines (A) Plant height; (B) Stem diameter; (C) Number of leaves; (D) Leaf length; (E) Leaf width; (F) Leaf area; (G) Biomass. L, M, and S are the same as shownin Figure 7. *, **, and *** indicate significant differences existing between the transgenic line and non-transgenic (NT) plant at 0.05, 0.01, and 0.001 levels, respectively (Student’s t test).

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异源表达异子蓬SaPEPC2基因提高烟草抗旱性和光合特性(长英文摘要）

Heterologous Expression of Suaeda aralocaspica SaPEPC2 Gene Improves Drought Resistance and Photosynthesis in Transgenic Tobacco

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