Lignin biosynthesis and accumulation in response to abiotic stresses in woody plants

Xiaojiao Han; Yanqiu Zhao; Yinjie Chen; Jing Xu; Cheng Jiang; Xiaqin Wang; Renying Zhuo; Meng-Zhu Lu; Jin Zhang; Xiaojiao Han; Yanqiu Zhao; Yinjie Chen; Jing Xu; Cheng Jiang; Xiaqin Wang; Renying Zhuo; Meng-Zhu Lu; Jin Zhang

doi:10.48130/FR-2022-0009

Figures (2) Tables (1)

Figure 1.
Schematic diagram summarizing the various abiotic stresses affecting lignin biosynthesis in woody plants. Phenylalanine ammonia lyase (PAL), cinnamate 4-hydroxylase (C4H), 4-coumarate:coenzyme A ligase (4CL), cinnamoyl-CoA reductase (CCR), caffeoyl-CoA O-methyltransferase (CCoAOMT), ferulate 5-hydroxylase (F5H), flavonoid 3-hydroxylase (F3H), caffeic acid O-methyltransferase (COMT), cinnamyl alcohol dehydrogenase (CAD), peroxidase (PRX), and laccase (LAC).
Figure 2.
Transcription factors in the lignin regulatory network involved in abiotic stress responses in herbaceous and woody plants. Genes in red dashed boxes represent orthologous genes in different species. Different colors show different abiotic stresses. Ft, Fagopyrum tataricum; Si, Setaria italic; Os, Oryza sativa; Ptr, Populus trichocarpa; Pto, Populus tomentosa; Md, Malus × domestica; Bp or Bpl, Betula platyphylla; Ej, Eriobotrya japonica; No prefix, Arabidopsis. AC element, SNBE site, HDE site, G-box, and HSE located on the promoter region of lignin biosynthetic genes represent the cis-acting elements for the binding of MYB, NAC, TF1L, bHLH and HSF transcrition factors, respectively.

Stress	Species	Tissue	Treatment	Main effects	Reference
Drought	Populus tomentosa	PtoMYB170-overexpressing Arabidopsis	Desiccated without watering for 2 weeks and then rewatered	Promoted lignin deposition by activating CCR2, COMT, CCoAOMT1 and C4H2	Xu et al.^[91]
	Populus trichocarpa	4-month-old OE-PtrbHLH186-L4 plants	Soil relative water content was reduced from 60% to 13% by withholding water	Transregulated many monolignol genes and increased in G subunits	Liu et al.^[85]
	Leucaena leucocephala	Stem and root	1% mannitol (w/v)	Increased lignification and corresponding CCR protein accumulation	Srivastava et al.^[16]
	Eucalyptus urograndis	Basal and apical regions of the stem	Not irrigated until wilt	Promoted lignin deposition and reduced the S/G ratio in the basal regions	Moura-Sobczak et al.^[12]
	Populus trichocarpa	Young shoot tissues (top 3 cm)	Supplying 150 ml water once per week for 4 weeks	Decreased the lignin S/G ratio in young shoots	Hori et al.^[17]
Flooding	Populus × canescens	Root	Water level of the containers exceeded the soil surface by 2 to 3 cm	Down-regulated lignin biosynthesis genes	Kreuzwieser et al.^[20]
Flooding	Syzygium samarangense	Root	The flooded pots maintained a depth of several centimeters of water in a plastic dish placed under the pots	Lignin accumulation in epidermis and cortex in both normal and flooded batches	Tuladhar et al.^[13]
Salt	Populus canescens and Populus euphratica	Leaf, stem, root	25 or 100 mM NaCl	Increased in the lignin: carbohydrate ratio in both species.	Janz et al.^[21]
	Betula platyphylla	Leaf of BpNAC012-overexpressing lines	200 mM NaCl	Elicited higher expression levels of lignin biosynthetic genes and elevated lignin accumulation in BpNAC012-overexpressing lines	Hu et al.^[79]
	Betula platyphylla	BplMYB46-overexpressing lines	200 mM NaCl for 10 d	BplMYB46 improved salt and osmotic tolerance by increasing lignin deposition	Guo et al.^[80]
	Malus × domestica	Leaf of MdSND1-overexpressing and MdSND1-RNAi lines	200 mM NaCl	MdSND1 is directly involved in the regulation of lignin biosynthesis.	Chen et al.^[78]
	Simmondsia chinensis	Leaf	50, 100 or 200 mM NaCl	Reduced lignin production	Alghamdi et al.^[23]
	Coffea arabica	Leaf	50, 100 or 150 mM NaCl	Cell walls of coffee leaves have undergone changes in the polysaccharide and lignin composition	de Lima et al.^[14]
	Tamarix hispida	Root	400 mM NaCl	Two genes SAMS and COMT involved in lignin synthesis were highly responsive to NaCl stress	Li et al.^[22]
Heat	Eriobotrya japonica	Fruit	40 °C	EjHSF1 trans-activated the lignin biosynthesis-related genes	Zeng et al.^[94]
Cold	Eriobotrya japonica	Fruit	0 or 5 °C	Chilling condition during postharvest storage lead to increased expression levels of PAL, 4CL and CAD, and resulted in increased lignin content	Liu et al.^[32]
	Populus tremula × P. tremuloides cv. Muhs1	Stem	10 °C	Increased lignin contents in cuttings	Hausman et al.^[33]
Heavy metals	Pinus sylvestris	Needles, stem, and roots	0.5, 1, 2, or 4 mM Al(NO₃)₃	Roots affected by Al showed deformation in cell walls and higher lignification and suberization.	Oleksyn et al.^[41]
	Citrus sinensis and Citrus grandis	Leaf, stem, root	1.0 mM AlCl₃·6H₂O	DCBC protein promoted the synthesis of lignin to achieve the ability to immobilize Al	Wu et al.^[45]
	Nine Myrtaceae species	roots	1.0 mM AlCl₃·6H₂O	Lignin was formed only in the root tips in Melaleuca bracteata	Tahara et al.^[40]
	Camellia sinensis	Root, leaf	Al₂(SO₄)₃·18H₂O	The down-regulation of F5H and the binding of Al and phenolic acids reduced the accumulation of lignin	Xu et al.^[44]
	Camellia sinensis	Roots or in cultured cells	400 µM AlCl₃	Reduced the activities of PAL and POD, and lignin content	Ghanati et al.^[43]
	Camellia sinensis	Callus Cultures	106 µM Cd(NO₃)₂	Increased the lignin content in the root and stem calli	Zagoskina et al.^[46]
	Avicennia schaueriana	Leaf, stem, root	0, 5, 15, 30, or 45 mg·L⁻¹ CdCl₂·5/2H₂O	Induced lignin deposition in xylem cells of all vegetative organs	Garcia et al.^[47]
	Populus × canescens	Leaf, wood, root	50 µM CdSO₄	Increased in GH3 activities and thereby shunted the metabolism to enhanced formation of lignin.	Elobeid et al.^[48]
	Scots pine (Pinus sylvestris)	Root	5 or 50 µM Cd	50 µM Cd resulted in significant increases in lignin content	Schützendübel et al.^[49]
	Two Salix caprea isolates	Root	0.5 mg·L⁻¹ CdNO₃·4H₂O	KH21 delayed the development of apoplastic barriers	Vaculík et al.^[53]
	Bruguiera gymnorrhiza and Rhizophora stylosa	Root, leaf	100, 200, 300, or 400 mg·kg⁻¹ CuCl₂	Increased lignification in mangroves roots	Cheng et al.^[60]
	Six species of mangroves	Root	400 µg·kg⁻¹ ZnCl₂, 200 µg·kg⁻¹ CuCl₂	Three high metal-tolerant rhizophoraceous species exhibited a thick exodermis with high lignification	Cheng et al.^[61]
Light	Pinus radiata	Callus cultures	From the dark to a 16 h photoperiod	Enhanced the enzymes CAD and PAL, and increased the amount of lignin	Möller et al.^[64]
	Malus domestica	Fruit	Direct sunlight, shaded, and severe sun damage	Induced the expression levels of MdCOMT1 and MdCAD in the flesh, and increased the accumulation of lignin in cell walls of the flesh and skin in sudden exposure	Torres et al.^[65]
	Fagus sylvatica	Leaf	Leaves of the sun and shade crown	Induced higher lignin contents in leaves in shade crown than in sun crown under ambient O₃ concentrations	Jehnes et al.^[62]
CO₂	Populus tremula × alba	Stems of young tree	Elevated CO₂ (800 µL·L⁻¹)	Increased lignin content in lower and middle stems	Richet et al.^[67]
	Betula pendula	Green leaves	Elevated CO₂ (2 × ambient)	Decreased contents of acid-soluble lignin in birch leaves	Oksanen et al.^[68]
	Fagus sylvatica	Two-year-old beech seedlings	Ambient and elevated CO₂	Leaves in the elevated CO₂ treatment contained less lignin than leaves in the ambient CO₂ treatment	Blaschke et al.^[69]

Table 1.

Effects of different abiotic stresses on lignin in woody plants.