Regulation of Lysine Uptake and Metabolism in Plants and Its Effects on Plants

doi:10.13304/j.nykjdb.2024.0155

Abstract

Abstract:

Lysine， a fundamental amino acid crucial for human and animal nutrition， also serves pivotal roles in amino acid homeostasis， growth， development， stress resilience and nutritional quality of plants. The biosynthesis， metabolic processes， absorption and translocation of lysine in plants directly or indirectly affect lysine content and its functions. While the metabolic pathways of lysine in plants have been relatively well characterized， the physiological and molecular mechanisms underlying its beneficial effects on plants remain largely unclear. In this paper， the recent advancements in understanding the roles and potential regulatory mechanisms of key genes involved in lysine uptake and metabolic pathways in plants were summarized， and the roles and possible regulatory mechanisms of key lysine absorption and metabolism genes in plant stress resistance， disease resistance， seed germination and improvement of crop quality were particularly elabrcted. Additionally， it reviewed the progress in breeding lysine-rich crops. Above results offered valuable insights and guidelines for elucidating the mechanisms regulating lysine transport and metabolism in cereal crops， thereby enhancing stress tolerance and fostering the development of novel lysine-enriched crop varieties.

Key words: lysine, amino acid transporter, uptake, metabolism, lysine-rich crops

摘要：

赖氨酸不仅是人类和动物的第一必需氨基酸，而且在维持植物体内氨基酸代谢平衡和生长发育、提高抗逆性与营养品质方面发挥着重要作用。植物赖氨酸合成代谢与吸收运输会直接或间接地影响植株赖氨酸含量及其功能。目前，对植物赖氨酸代谢调控通路的解析已比较清晰，但赖氨酸对植物产生积极影响的分子机理尚不清楚。系统梳理了近些年赖氨酸吸收及其合成代谢途径，重点阐述了赖氨酸吸收与代谢关键基因在植株抗逆性、抗病性、种子萌发和提高作物品质等方面的作用及可能调控机制，以及赖氨酸作物育种策略的研究进展，以期为揭示谷类作物赖氨酸的吸收与代谢调控机制、提高植物抗逆能力和营养品质以及改良培育富赖氨酸作物新品种提供理论依据。

关键词: 赖氨酸, 氨基酸转运体, 吸收, 代谢, 富赖氨酸作物

CLC Number:

Q945.12

Kexin WANG, Yuehua DONG, Xuanyi HE, Huaiyu YANG. Regulation of Lysine Uptake and Metabolism in Plants and Its Effects on Plants[J]. Journal of Agricultural Science and Technology, 2025, 27(7): 20-29.

王可欣, 董月华, 何炫颐, 杨怀玉. 植物赖氨酸吸收与代谢调控及对植物的影响[J]. 中国农业科技导报, 2025, 27(7): 20-29.

Figures/Tables 3

References 67

[1]	YONEYAMA T, SUZUKI A.Light-independent nitrogen assimilation in plant leaves:nitrate incorporation into glutamine, glutamate, aspartate, and asparagine traced by 15N [J/OL]. Plants, 2020,9(10):1303 [2024-02-06]..
[2]	TEGEDER M, MASCLAUX-DAUBRESSE C.Source and sink mechanisms of nitrogen transport and use [J]. New Phytol., 2018,217(1):35-53.
[3]	杨晴晴,吴宏玉,陈思予,等. 高等植物中赖氨酸代谢调控及其关联效应研究进展[J]. 植物生理学报. 2019, 55(12): 1737-1746.
	YANG Q Q, WU H Y, CHEN S Y, et al.. Advances in regulation and connection of lysine metabolism in higher plants [J]. Plant Physiol. J., 2019, 55(12): 1737-1746.
[4]	田颖,时明慧.赖氨酸生理功能的研究进展[J].美食研究,2014,31(3):60-64.
	TIAN Y, SHI M H. The research progress of the physiologic functions of lysine [J]. J.Res. Diet. Sci. Culture, 2014,31(3):60-64.
[5]	YANG Q, ZHAO D, ZHANG C, et al.. Lysine biofortification of crops to promote sustained human health in the 21st century [J]. J. Exp. Bot., 2022,73(5):1258-1267.
[6]	SU Y H, FROMMER W B, LUDEWIG U. Molecular and functional characterization of a family of amino acid transporters from Arabidopsis [J]. Plant Physiol., 2004,136(2):3104-3113.
[7]	CHEN L, BUSH D R.LHT1,a lysine- and histidine-specific amino acid transporter in Arabidopsis [J]. Plant Physiol., 1997,115(3):1127-1134.
[8]	WANG J, WU B W, LU K, et al.. The amino acid permease 5 (OsAAP5) regulates tiller number and grain yield in rice [J].Plant Physiol., 2019,180(2):1031-1045.
[9]	FROMMER W B, HUMMEL S, UNSELD M, et al.. Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis [J].Insects, 1995,92(26):12036-12040.
[10]	YANG H, POSTEL S, KEMMERLING B, et al.. Altered growth and improved resistance of Arabidopsis against Pseudomonas syringae by overexpression of the basic amino acid transporter AtCAT1 [J]. Plant Cell Environ., 2014,37(6):1404-1414.
[11]	HIRNER A, LADWIG F, STRANSKY H, et al.. Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll [J]. Plant Cell, 2006,18(8):1931-1946.
[12]	TEGEDER M, WARD J M. Molecular evolution of plant AAP and LHT amino acid transporters [J/OL]. Front. Plant Sci., 2012, 3: 21 [2024-02-06]. .
[13]	WANG X, YANG G, SHI M, et al.. Disruption of an amino acid transporter LHT1 leads to growth inhibition and low yields in rice [J/OL]. BMC Plant Biol., 2019,19(1):268 [2024-02-06]..
[14]	LI Z, GAO J, WANG S, et al.. Comprehensive analysis of the LHT gene family in tobacco and functional characterization of NtLHT22 involvement in amino acids homeostasis [J/OL].Front. Plant Sci., 2022,13:927844 [2024-02-06]. .
[15]	SVENNERSTAM H, JÄMTGÅRD S, AHMAD I, et al.. Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations [J]. New Phytol., 2011,191(2):459-467.
[16]	FISCHER W N, LOO D D, KOCH W, et al.. Low and high affinity amino acid H⁺-cotransporters for cellular import of neutral and charged amino acids [J]. Plant J., 2002,29(6):717-731.
[17]	HUNT E, GATTOLIN S, NEWBURY H J, et al.. A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected [J]. J. Exp. Bot., 2010,61(1):55-64.
[18]	TAYLOR M R, REINDERS A, WARD J M. Transport function of rice amino acid permeases (AAPs) [J]. Plant Cell Physiol.,2015, 56(7):1355-1363.
[19]	FENG L, YANG T Y, ZHANG Z L, et al.. Identification and characterization of cationic amino acid transporters (CATs) in tea plant (Camellia sinensis) [J]. Plant Growth Regul., 2018,84(1):57-69.
[20]	AZEVEDO R A, LEA P J. Lysine metabolism in higher plants [J]. Amino Acids, 2001,20(3):261-279.
[21]	ARRUDA P, KEMPER E L, PAPES F, et al.. Regulation of lysine catabolism in higher plants [J]. Trends Plant Sci., 2000,5(8):324-330.
[22]	HARTMANN M, ZEIER T, BERNSDORFF F, et al.. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity [J]. Cell, 2018,173(2):456-469.
[23]	UMBARGER H E. Amino acid biosynthesis and its regulation [J]. Ann. Rev. Biochem., 1978, 47(1): 533-606.
[24]	PARIS S, WESSEL P M, DUMAS R.Overproduction,purification,and characterization of recombinant aspartate semialdehyde dehydrogenase from Arabidopsis thaliana [J]. Protein Exp. Purif., 2002,24(1):99-104.
[25]	于妍,宋万坤,刘春燕,等.植物天冬氨酸代谢途径关键酶基因研究进展[J].生物技术通报,2008():7-11, 17.
	YU Y, SONG W K, LIU C Y, et al.. Research development of key enzymes gene on aspartic acid metabolic pathway in plants [J]. Biotechnol. Bull., 2008(S1):7-11, 17.
[26]	杨晴晴.高赖氨酸转基因水稻的营养评价及代谢关联研究[D].扬州:扬州大学,2016.
	YANG Q Q. Nutritional assessment and metabolic connection analysis of transgenic rice with high free lysine [D]. Yangzhou:Yangzhou University, 2016.
[27]	PERL A, SHAUL O, GALILI G. Regulation of lysine synthesis in transgenic potato plants expressing a bacterial dihydrodipicolinate synthase in their chloroplasts [J]. Plant Mol.Biol., 1992,19(5):815-823.
[28]	DUNHAM V L, BRYAN J K. Synergistic effects of metabolically related amino acids on the growth of a multicellular plant [J]. Plant Physiol., 1969, 44(11): 1601-1608.
[29]	CRACIUN A, JACOBS M, VAUTERIN M. Arabidopsis loss-of-function mutant in the lysine pathway points out complex regulation mechanisms [J]. Sci. Rep., 2000,487(2): 234-238.
[30]	VAN BOCHAUTE P, NOVOA A, BALLET S, et al.. Regulatory mechanisms after short- and long-term perturbed lysine biosynthesis in the aspartate pathway:the need for isogenes in Arabidopsis thaliana [J]. Physiol. Plant., 2013,149(4): 449-460.
[31]	BLICKLING S, BEISEL H G, BOZIC D,et al..Structure of dihydrodipicolinate synthase of Nicotiana sylvestris reveals novel quaternary structure [J].J. Mol. Biol., 1997,274(4):608-621.
[32]	LEE S I, KIM H U, LEE Y H, et al.. Constitutive and seed-specific expression of a maize lysine-feedback-insensitive dihydrodipicolinate synthase gene leads to increased free lysine levels in rice seeds [J]. Mol. Breed., 2001,8(1):75-84.
[33]	SHAVER J M, BITTEL D C, SELLNER J M, et al.. Single-amino acid substitutions eliminate lysine inhibition of maize dihydrodipicolinate synthase [J]. Proc. Natl. Acad. Sci. USA,1996,93(5):1962-1966.
[34]	SODEK L, WILSON C M. Incorporation of leucine-14C and lysine-14C into protein in the developing endosperm of nomal and opaque-2 corn [J]. Arch.Biochem. Biophys.,1970,140(1):29-38.
[35]	BRANDT A B. In vivo incorporation of (14C) lysine into the endosperm proteins of wild type and high-lysine barley [J]. FEBS Lett., 1975, 52(2): 288-291.
[36]	HARTMANN M, ZEIER J. l-lysine metabolism to N-hydroxypipecolic acid: an integral immune-activating pathway in plants [J]. Plant J., 2018, 96(1): 5-21.
[37]	JANCEWICZ A L, GIBBS N M, MASSON P H. Cadaverine’s functional role in plant development and environmental response [J/OL]. Front. Plant Sci.,2016,7:870 [2024-02-06]..
[38]	NÁVAROVÁ H, BERNSDORFF F, DÖRING A C, et al.. Pipecolic acid,an endogenous mediator of defense amplification and priming,is a critical regulator of inducible plant immunity [J]. Plant Cell, 2013,24(12):5123-5141.
[39]	ANDERSON O D, COLEMAN-DERR D, GU Y Q, et al.. Structural and transcriptional analysis of plant genes encoding the bifunctional lysine ketoglutarate reductase saccharopine dehydrogenase enzyme [J/OL]. BMC Plant Biol., 2010,10:113 [2022-02-06]. .
[40]	REYES A R, BONIN C P, HOUMARD N M, et al.. Genetic manipulation of lysine catabolism in maize kernels [J]. Plant Mol. Biol., 2009,69(1):81-89.
[41]	BROCKER C, LASSEN N, ESTEY T, et al.. Aldehyde dehydrogenase 7A1 (ALDH7A1) is a novel enzyme involved in cellular defense against hyperosmotic stress [J]. J. Biol. Chem., 2010, 285(24): 18452-18463.
[42]	RODRIGUES S M, ANDRADE M O, GOMES A P S, et al.. Arabidopsis and tobacco plants ectopically expressing the soybean antiquitin-like ALDH7 gene display enhanced tolerance to drought,salinity,and oxidative stress [J]. J. Exp. Bot., 2006, 57(9): 1909-1918.
[43]	SHIN J H, KIM S R, AN G. Rice aldehyde dehydrogenase 7 is needed for seed maturation and viability [J]. Plant Physiol., 2009,149(2): 905-915.
[44]	GROBBELAAR N, STEWARD F C. Pipecolic acid in Phaseolus vulgaris: evidence on its derivation from lysine [J]. J.Am. Chem. Soc., 1953,75(17):4341-4343.
[45]	ZEIER J. New insights into the regulation of plant immunity by amino acid metabolic pathways [J]. Plant Cell Environ., 2013,36(12):2085-2103.
[46]	MISHINA T E, ZEIER J. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance [J]. Plant Physiol., 2006,141(4):1666-1675.
[47]	BUNSUPA S, YAMAZAKI M, SAITO K. Quinolizidine alkaloid biosynthesis:recent advances and future prospects [J/OL].Front. Plant Sci., 2012,3:239 [2024-02-06]. .
[48]	HILDEBRANDT T M. Synthesis versus degradation:directions of amino acid metabolism during Arabidopsis abiotic stress response [J]. Plant Mol. Biol., 2018,98(1):121-135.
[49]	KIYOTA E, PENA I A, ARRUDA P. The saccharopine pathway in seed development and stress response of maize [J]. Plant Cell Environ., 2015,38(11):2450-2461.
[50]	MOULIN M, DELEU C, LARHER F, et al.. The lysine-ketoglutarate reductase-saccharopine dehydrogenase is involved in the osmo-induced synthesis of pipecolic acid in rapeseed leaf tissues [J]. Plant Physiol. Biochem., 2006,44(7-9):474-482.
[51]	YANG H, LUDEWIG U. Lysine catabolism,amino acid transport,and systemic acquired resistance:what is the link? [J/OL].Plant Signal. Behav., 2014,9(7):e28933 [2024-02-06]..
[52]	LIU G S, JI Y Y, BHUIYAN N H,et al.. Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis [J].Plant Cell, 2010,22(11): 3845-3863.
[53]	MOORMANN J, HEINEMANN B, HILDEBRANDT T M. News about amino acid metabolism in plant-microbe interactions [J]. Trends Biochem. Sci., 2022,47(10):839-850.
[54]	ANZALA F, MORERE-LE PAVEN M C, BIROLLEAU-TOUCHARD C, et al.. QTL mapping and genetic analysis of inhibitory effect of lysine on post- germination growth and seedling establishment of maize [J]. Acta Agron. Hungarica, 2006, 54(3): 271-279.
[55]	GALILI G, AMIR R. Fortifying plants with the essential amino acids lysine and methionine to improve nutritional quality [J].Plant Biotechnol. J., 2013,11(2):211-222.
[56]	WHO. Protein and amino acid requirements in human nutrition [J]. World Health Organ.Tech.Rep.Ser., 2007,935:1-265.
[57]	ZHU X H, GALILI G. Lysine metabolism is concurrently regulated by synthesis and catabolism in both reproductive and vegetative tissues [J]. Plant Physiol., 2004,135(1):129-136.
[58]	DHATTERWAL P, MEHROTRA S, MILLER A J, et al.. Promoter profiling of Arabidopsis amino acid transporters:clues for improving crops [J]. Plant Mol. Biol., 2021,107(6):451-475.
[59]	MERTZ E T, BATES L S, NELSON O E. Mutant gene that changes protein composition and increases lysine content of maize endosperm [J]. Science, 1964,145(3629):279-280.
[60]	SARIKA K, HOSSAIN F, MUTHUSAMY V, et al.. Marker-assisted pyramiding of opaque 2 and novel opaque16 genes for further enrichment of lysine and tryptophan in sub-tropical maize [J]. Plant Sci., 2018,272:142-152.
[61]	YUE J, LI C, ZHAO Q, et al.. Seed-specific expression of a lysine-rich protein gene,GhLRP,from cotton significantly increases the lysine content in maize seeds [J]. Int. J. Mol. Sci., 2014,15(4):5350-5365.
[62]	YANG Q Q, YU W H, WU H Y, et al.. Lysine biofortification in rice by modulating feedback inhibition of aspartate kinase and dihydrodipicolinate synthase [J]. Plant Biotechnol. J., 2021,19(3):490-501.
[63]	TANG M, HE X, LUO Y, et al.. Nutritional assessment of transgenic lysine-rich maize compared with conventional quality protein maize [J]. J. Sci. Food Agric., 2013,93(5):1049-1054.
[64]	HENRY C J. Functional foods [J]. Eur. J. Clin. Nutr., 2010, 64(7): 657-659.
[65]	SENARATHNA S, MEL R, MALALGODA M. Utilization of cereal-based protein ingredients in food applications [J/OL]. J. Cereal Sci.,2024,116:103867 [2024-02-06]..
[66]	MOYA M. Lysine genetically enriched cereals for improving nutrition in children under 5 years in low- and middle-income countries [J]. J. Nutr. Health Food Eng., 2016, 5(2): 583-586.
[67]	HE L, SUI Y, CHE Y, et al.. New insights into the genetic basis of lysine accumulation in rice revealed by multi-model GWAS [J/OL]. Int. J. Mol. Sci., 2024,25(9):4667 [2024-02-06]. .