Plant protein-coding gene families: Their origin and evolution

Abstract

Steady advances in genome sequencing methods have provided valuable insights into the evolutionary processes of several gene families in plants. At the core of plant biodiversity is an extensive genetic diversity with functional divergence and expansion of genes across gene families, representing unique phenomena. The evolution of gene families underpins the evolutionary history and development of plants and is the subject of this review. We discuss the implications of the molecular evolution of gene families in plants, as well as the potential contributions, challenges, and strategies associated with investigating phenotypic alterations to explain the origin of plants and their tolerance to environmental stresses.

Introduction

The driving force underlying biological evolution is environmental selection. The criteria for plant diversification include marked interspecific phenotypic and genetic differences, which can be accompanied by marked reproductive isolation. However, by its very nature, plant evolution is a process wherein variations occur based on the presence, composition, and number of genes (Lafon-Placette et al., 2016). Interestingly, throughout this process, several important evolutionary mechanisms have dominated. These mechanisms include changes in drought resistance and oxygen uptake due to adaptation of plants to life on land (“landing”), formation of root and vascular structures, and evolution of metabolites in response to stress hazards. Additionally, co-evolution of floral structures has occurred in parallel with insects, leading to the co-evolution of insect mouthparts and floral diversity. Indeed, selected traits are often closely associated with the generation, development, and functional specialization of specific gene families (Gramzow et al., 2010; Cheng et al., 2019; Nikolov et al., 2019).

Horizontal gene transfer (HGT) may contribute to the adaptation of plants to life on land (Cheng et al., 2019), and has been documented in various gene families (Preston and Hileman, 2013; Shao et al., 2019). Moreover, several gene families are associated with repeated events, including tandem replication, fragment replication, wide-genome duplication (WGD), and transposable replication, leading to significant functional or phenotypic differences among plants (Wang et al., 2019, 2020; Schilling et al., 2020). For example, transposable replication often results in the formation of pseudogenes, while other types of replications cause a rapid expansion of plant genomes, leading to severe functional redundancy and increased functional differentiation in plant gene families. The presence of these redundant genes leads to a more complex adaptive system that drives plant-gene-phenotype-environment interactions, resulting in sub functionalization or de novo functionalization of these genes. This enables a coordinated and robust molecular network of environmental regulation in plants (Duplais et al., 2020; Man et al., 2020; Schilling et al., 2020).

A gene family is a group of genes with a common origin that encode proteins with similar structural properties and biochemical functions. Several key gene families, including MADS (Mcml Agamous Deficiens Srf-box domain gene family), CYP (Cytochrome P450 protein family), and HSP (Heat Shock Protein family), are core promoters of plant metabolism and flower formation (Ng and Yanofsky, 2001; Nelson and Werck-Reichhart, 2011; Bondino et al., 2012). For example, in the “ABCDE” model of flower development, the MADS-box genes are divided into two groups, namely, M-type_MADS and MIKC_MADS, with the latter considered to be the main contributor to flower development (Airoldi and Davies, 2012; Theissen et al., 2016; Hsu et al., 2021). In addition, evolutionary studies suggest extensive functional differentiation within these gene families and subfamilies. For example, the CYP gene family can be divided into two groups: type A-encoding genes, which encode oxygenases acting in pathways for the synthesis of plant-specific metabolites, including many chemosensory substances and drug components, and non-type A-encoding genes, which encode oxygenases required for the synthesis of more basic plant metabolites, such as endogenous plant hormones and essential metabolites (Ng and Yanofsky, 2001; Nelson and Werck-Reichhart, 2011; Airoldi and Davies, 2012; Theissen et al., 2016; Hsu et al., 2021; Su et al., 2021). Knowledge of the functional roles of plant gene families is vital to our understanding of plant evolution.

However, due to the richness of species and the associated wide range of gene families, the evolution of most gene families is poorly documented. This limits our in-depth exploration of plant origin and differentiation, as well as the application of molecular genetics. Therefore, evolutionary studies have taken a more comprehensive, multispecies approach.

Plant evolution

The evolution of plants from primitive plant ancestors has been largely simplified to red algae to green algae (basic green plants), mosses (basic land plants), ferns (basic vascular plants), gymnosperms (basic seed plants), and angiosperms. During this process, the phenotypes and genotypes of algae, mosses, ferns, and seed plants varied considerably. At the phenotypic level, selection of characteristics, such as plant type, leaf shape, and floral organs, is influenced by animal behavior, human activities, as well as climatic factors, leading to broad phenotypic diversity (Figure 1). At the genotypic level, abundant genetic changes such as WGD, tandem repeats, transposition, gene loss, and parallel gene transfer contribute significantly to the diversity of protein-coding plant genes and selective responses to the environment (Gramzow et al., 2010; Preston and Hileman, 2013; Cheng et al., 2019; Nikolov et al., 2019; Shao et al., 2019; Schilling et al., 2020).

FIGURE 1.

Plant evolution. The symbiosis of dinoflagellate protists with cyanobacteria prompted the occurrence of phytoplanktonic communities, with diverse phytoplanktonic taxa (including plants, green algae, red algae, and cryptophytes) arising through biological adaptation to the environment. At the origin of green algae and Streptophytina, significant differences in drought and oxygen stress tolerance developed to facilitate terrestrialization. During the process of adaptation to the environment, certain taxa underwent unique adaptations in root, flower, and other related phenotypes, which in turn ensured the dominance of the widely distributed angiosperms.

Although the origin of terrestrial plants remains controversial, Cheng et al. (2019) reported that land plants might have originated from two Zygnematophyceae species, namely, Spirogloea muscicola and Mesotaenium endlicherianum. Cheng et al. (2019) and Liang et al. (2020) further reported that two species from outside the Streptophytina—Mesostigma viride and Chlorokybus atmophyticus—may represent the most primitive branches of terrestrialized plants. Further, genomic analysis identified Prasinodermaphyta as a potential new phylum between the green and red algal phyla (Li et al., 2020). Meanwhile, molecular analyses have revealed that mosses originated approximately 908–680 million years ago (Mya), suggesting that the origin of land plants occurred earlier than the Ordovician (Sun et al., 2021). Additionally, comparison of the genomes of magnolias indicates that Magnoliids and monocotyledons form a unique monophyletic group that may appear earlier than either the monocotyledon or the Austrobaileyales, Nymphaeales, and Amborellales (ANA) branches (Dong et al., 2021).

Based on genomic and transcriptomic analysis of representative bryophytes (including liverworts, hornworts, and mosses), Gao et al. (2020) noted that polyploidy was common in bryophytes. Polyploidization events occurred in bryophyte ancestors before differentiation, as well as within Funarioideae ancestors, and Buxbaumiidae, Diphysciidae, Timmiidae, and Funariidae branches. Schneider et al. (2017) found that polyploidization plays an important role in fern diversity. In fact, several instances of polyploidization contributed to the diversity of Asplenium plants, with ploidy levels of 2* and 4* being the most common. Meanwhile, two of the oldest polyploidization events were reported in seed plants (192 Mya) and angiosperms (319 Mya), during which genome multiplication was a hallmark of the evolution of angiosperms from gymnosperms (Schneider et al., 2017). In basal angiosperms, the ANA branch of camphor and water lily genomes indicates a polyploidization event in the water lily ancestor (Zhang et al., 2019). Similarly, magnolia genomes indicate that one polyploidization event occurred during their ancestry, while two additional polyploidization events occurred in Lauraceae. Wang et al. (2019) and Zhang L. S. et al. (2020) systematically organized the abundant polyploidy of angiosperms and confirmed that monocotyledonous plants from the Gramineae (100–110 Mya) and Lemnaceae (115–125 Mya) families are highly polyploid. Specifically, the orders Poales and Arecales appear to have had one polyploidization event, whereas plantains arose from three polyploidization events over a short period. Indeed, dicotyledonous plants are usually paleohexaploid (gamma triplication; 115–130 Mya), including Malvaceae, Brassicaceae, Cucurbitaceae, and Leguminosae, all of which originated following multiple ploidy events (Wang et al., 2019). Importantly, abundant gene duplications have also been reported in the genomes of other angiosperms, including sugarcane, kiwifruit, and tea tree (Vilela et al., 2017; Wang et al., 2018).

Overview of plant gene families

A plant gene family refers to a group of genes with related functions that are generated by gene duplication from a single-copy gene source in an ancestor, and retain similar sequence and structure (Li et al., 2022). Gene families can be associated with repeated events, such as tandem replication, fragment replication, WGD, or transposable replication, based on the scope of replication, size of the replicated region, and influence of transposons (Airoldi and Davies, 2012; Su et al., 2021). Transposable replication is one such event that often leads to formation of pseudogenes, while other types of replications cause a rapid expansion of plant genomes, leading to severe functional redundancy and increased functional differentiation within plant gene families (Schilling et al., 2020; Yu et al., 2020).

Plant genomes include protein-coding and non-coding RNA (ncRNA) gene families (Song et al., 2021; Li et al., 2022). Gene families encoding ncRNA can be further subdivided into those encoding lncRNA (long non-coding RNA), miRNA (micro RNA), rRNA (ribosomal RNA), tRNA (transfer RNA), and circRNA (circular RNA), and will not be further discussed here. Protein-coding gene families can also be broadly classified by the function of the proteins they encode, including receptors, kinases, epigenetic modification, structural, and transcription factors (TFs) (Figure 2A). However, these classifications are not unique; gene families can also be divided into several categories depending upon the classification criteria, such as classifications based on function, structural features, or the pathways involved. Hence, the class of chloroplast transporters TOC-TIC can be classified as either membrane proteins or structural proteins, whereas G-protein-coupled signal receptors can be classified as either membranes or receptor proteins. Many gene families within plant genomes are unique to plants, including more than 57 families of TFs, e.g., the TEOSINTE BRANCHED 1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP), and SQUAMOSA PROMOTER-BINDING PROTEIN (SBP) families (Figure 2B; Reeves and Olmstead, 2003; Yang et al., 2008; Preston and Hileman, 2013; Jin et al., 2017; Wu et al., 2017).

FIGURE 2.

Plant gene families. (A) A brief classification of gene families found in plants. (B) A rich taxonomy of plant transcription factors. tRNA is an RNA composed of 76–90 nucleotides that carry amino acids into the ribosome and synthesize proteins under the guidance of mRNA; lnc RNA is a class of non-coding RNA molecules longer than 200 nt; mi RNA is a class of endogenous, small RNAs of about 20–24 nucleotides in length; circ RNA is a class of RNAs that do not have a 5′ terminal cap and 3′ terminal poly(A) tail, and are covalently bonded to form a loop structure; they are a class of non-coding RNA molecules that are found in living organisms. cnc RNA (coding and non-coding RNA) is a family of functional genes that can be differentially sheared in a variable manner, resulting in both short peptides or small molecular weight proteins and untranslatable functional RNAs (e.g., Inc RNA, mi RNA, etc.).

Evolution of gene families in plants

Evolution of resistance gene families

Resistance genes are groups of genes encoding proteins required for tolerance or immunity during plant adaptation to adverse external stress. Multiple environmental stresses have driven the molecular selection of these genes. Resistance gene clusters such as the NBS-LRR family are large and exhibit a high degree of functional differentiation (Shao et al., 2019). HSP and sHSP encode important heat-responsive proteins and molecular chaperones, and the copy number of sHSPs is significantly increased in polyploid plants with multiple branches. Genes from different subclasses may have diversified in function (Bondino et al., 2012). In contrast, the molecular chaperone gene PFDN, which displays only marginal differences between different groups, is expanded in polyploid plants such as soybean (Cao et al., 2016). Furthermore, the number of chilling injury-related gene (CRG) family members in Cruciferae is affected by polyploidy (Song et al., 2020). On the other hand, evolution of the AOX gene family is primarily mediated by intron/exon loss or gain, and fragment deletion, although gene loss and duplication, as well as tandem blocking, also play essential roles in the origin and maintenance of the family (Pu et al., 2015; Tables 1, 2; Figure 3).

TABLE 1.

Structural analysis of plant protein-coding gene families.

Gene family	Abbreviation	Major function	Domain	References
Metabolic enzymes
Cytochrome P450	CYP/P450	Monooxygenation activity	P450	Su et al., 2021
12-oxo-phytodienoate acid reductase	OPR	Jasmonic acid biosynthesis	Unknown	Guo et al., 2016
3-hydroxy-3-methylglutaryl Coenzyme A Reductase	HMGR	Terpene synthesis	PF00368	Li et al., 2014
Aconitase	ACO	Catalyzes the Isomerization of citrate to isocitrate	ACO	Wang et al., 2016
3-ketoacyl-coa synthase	KCS	Very long-chain fatty acids (VLCFAS) synthesis	ACP synthase III C and like	Guo et al., 2016
Antiviral gene cluster
Leucine-rich repeats Receptor-like protein kinases	LRR-RLK	Perceptual signaling and phosphorylation	LRR and RLK	Man et al., 2020
Argonaute	AGO	Antiviral activity	PAZ and Piwi	Singh et al., 2015
Double stranded RNA binding protein	DRB	Antiviral activity	DSRM	Clavel et al., 2016
Thaumatin-like protein	TLP	Plant disease resistance	TLP	Cao et al., 2016
Nucleotide-binding leucine-rich repeat	NLR	Plant disease resistance	NB-ARC	Borrelli et al., 2018
Nucleotide binding site leucine-rich repeat	NBS-LRR	Plant disease resistance	LRR and NBS	Shao et al., 2019
Transcription factor cluster
\	MADS	Flower development	MADS	Gramzow et al., 2010
AT-hook Motif Nuclear Localized	AHL	Organ development and bulky	AT-hook and PPC	Zhao et al., 2014
Arabidopsis LSH1 and Oryza G1	ALOG	Regulate reproductive growth	Unknown	Naramoto et al., 2020
Auxin/Indole Acetic Acid and Auxin Response Factor	Aux/IAA	Auxin response	Aux/IAA	Wu et al., 2017
Cysteine-rich polycomb-like protein	CPP-like	Development of reproductive organs	CXC	Yang et al., 2008
Wuschel-related	WOX	Regulating cell division and differentiation	WOX	Lian et al., 2014
Class III Homeodomain-Zine finger protein	C3HDZ	Leaf growth	HD-ZIP	Vasco et al., 2016
\	YABBY	Leaf growth	YABBY	Finet et al., 2016
\	3R-MYB	Drought and development	3 MYB	Feng et al., 2017
Anti-stress gene cluster
Small heat shock protein/alpha-crystallin	sHSP/Cry	Molecular chaperone	HSP20	Bondino et al., 2012
Prefoldin	PFDN	Molecular chaperone	Prefoldin	Cao, 2016
Cold-related genes	CRG	Cold-related	Unknown	Song et al., 2020
Alternative oxidase	AOX	Ubiquinol to reduce oxygen to water	Unknown	Pu et al., 2015
Structural composition or organogenesis gene cluster
SH3 and BAR domain-containing protein	SH3P	The Plant Cell Division and Autophagy	BAR domain	Forero and Cvrckova, 2019
Hairy meristem	HAM	Meristem formation	GRAS	Geng et al., 2021
Cellulose synthase	CesA	Cellulose synthesis	Cellulose_synt, Glycos_transf_2 and Glyco_trans_2_3	Little et al., 2018
Flowering locus t/terminal flower 1	FT/TFLl	Flower development	Unknown	Jin et al., 2021
Myosin	Myo	Actin system	Unknown	Peremyslov et al., 2011
Alternative splicing modulators nuclear speckle rna-binding proteins	NSR/RBP	Gene expression	Unknown	Lucero et al., 2020
Cyclin	Cyc	Cycle control	Cyclin_N and Cyclin_C	Boscolo-Galazzo et al., 2021
OVATE family protein	OFP	Fruit shape regulation	OVATE	Liu et al., 2014
Aquaporins	AQP	Water inflow and cycle control	Unknown	Hussain et al., 2020
Dynein light chain	DLC	Dynein complexes	4 helix and 4 sheet	Cao et al., 2017
Psbp protein	PsbP	Oxygen-evolving complex (OEC)	I and II	Ifuku et al., 2008
Signal-mediated gene clusters
Calcineurin B-Like and CBL-Interacting Protein Kinase	CBL/CIPK	Ca2+ signal	CBL/CIPK/C2	Zhang X. X. et al., 2020
Calcium-dependent protein kinase and CDPK-related kinase	CDPK/CRK	Ca2+ signal	CDPK/CRK/C2	Xiao et al., 2017
Glycerol-3-phosphate acyltransferase	GPAT	Phospholipid signal	acyltransferase	Waschburger et al., 2018
Phosphatidyl ethanolamine binding protein	PEBP/MFT-like	Phospholipid signal	Unknown	Hedman et al., 2009; Karlgren et al., 2011
Rapid alkalization factor	RALF	PH rise induction	Unknown	Cao and Shi, 2012
Auxin response factor	ARF	Auxin signal transduction	ARF	Finet et al., 2013
Cyclic nucleotide-gated ion channel	CNGC	Calcium signal transduction	CNB	Saand et al., 2015
C-terminally encoded peptide	CEP	Small secreted peptide signals	CEP	Ogilvie et al., 2014
Poly(A)-binding protein	PAB	Promoting mrna integrity and protein synthesis	PABP	Gallie and Liu, 2014
Supply of nutrients or ions gene clusters
Vacuolar iron transporter	VIT	Iron sensing and transport	VIT	Cao, 2019
Ferritin	Fer	Iron sensing and transport	Unknown	Strozycki et al., 2010
H+-ppase	VP	Proton-translocating pyrophosphatase	TM1-16	Zhang Y. M. et al., 2020
Phosphate 1	PHO	Inorganic phosphate (Pi) sensing and transport	SPX, EXS	He et al., 2013
Cobalamin-independent methionine synthase	CIMS	Cobalamin-independent methionine synthase	Unknown	Rody and de Oliveira, 2018
Hydrolase gene clusters
B -amylase	BAM	Glucan hydrolytic	Unknown	Thalmann et al., 2019
Sucrose synthase	SUS	Sugar hydrolysis	Unknown	Xu et al., 2019
Apparent components gene clusters
Histone methyltransferases	HMT	Methylation process	Unknown	Zhao et al., 2018
F-box	FBP	Ubiquitylation process	F-box	Navarro-Quezada et al., 2013

Major function indicates the most important functional role of gene families; domain refers to a conserved region of a protein sequence that may be related to the functional site of the protein. Some gene families are marked with a domain labeled “Unknown” to denote that a specific model of their overall structure is not currently known, and the methods available for further discovery of new sequences can only rely on the appropriate “blast p” homology search. For such proteins, a larger scale phylogenetic exploration may be useful to infer and resolve their function and structure.

TABLE 2.

Evolutionary events of plant protein-coding gene families.

Gene family	Numbers	Coverage	Copy event	Contribution to genome-wide repeating events	Stage of event	References
Metabolic enzymes
CYP/P450	251	Unknown	Order level and below level	B1	Unknown	Su et al., 2021
OPR	6	A1, 11	Order level and below level	B1	Chlorophyta, unknown	Li et al., 2009
HMGR	2	A1, 20	Species level	B1	Moss, unknown	Li et al., 2014
ACO	3	A2, 12	Species level	B1	Unknown	Wang et al., 2016
KCS	11	A1, 28	Order level and below level	B1	Chlorophyta, unknown	Li et al., 2009
Antiviral
LRR-RLK	225	A2, 9	Species level	B1	Unknown	Man et al., 2020
AGO	10	A1, 30	Order level and below level	B1	Chlorophyta, unknown	Singh et al., 2015
DRB	7	A5, 15	Species level	B1	Unknown	Clavel et al., 2016
TLP	24	A1, 6	Order level and below level	B1	Chlorophyta, unknown	Cao et al., 2016
NLR	144	A5, 3	Species level	B1	Unknown	Borrelli et al., 2018
NBS-LRR	204	A0, 79	Order level and below level	B1	Chlorophyta, unknown	Shao et al., 2019
Transcription factors
MADS	43	A0, Unknown	Order level and below level	B1	Earlier, MRCA	Gramzow et al., 2010
AHL	29	A1, 19	Order level and below level	B1	Moss, unknown	Zhao et al., 2014
ALOG	10	A1, 9	Order level and below level	B1	Chlorophyta, ALOS1	Naramoto et al., 2020
Aux/IAA	29	A1, 17	Order level and below level	B1	Moss, unknown	Wu et al., 2017
CPP-like	8	A4, 2	Unknown	B0	Unknown	Yang et al., 2008
WOX	16	A0, 50	Order level and below level	B1	Chlorophyta, unknown	Lian et al., 2014
C3HDZ	5	A1, 32	Order level and below level	B1	Chlorophyta, unknown	Vasco et al., 2016
YABBY	6	A3, 50	Species level	B1	Unknown	Finet et al., 2016
3R-MYB	5	A1, 65	Order level and below level	B1	Chlorophyta, unknown	Feng et al., 2017
Anti-stress
sHSP/Cry	27	A4, 17	Species level	B1	Unknown	Bondino et al., 2012
PFDN	9	A1, 14	Family level	B1	Chlorophyta, unknown	Cao et al., 2016
CRG	420	A2, 21	Species level	B1	Unknown	Song et al., 2020
AOX	5	A1, Unknown	Order level and below level	B1	Charophyta, AOX1 and AOX2	Pu et al., 2015
Structural composition or organogenesis
SH3P	3	A1, 20	Family level of angiosperms	B0	Charophyta, SH3P1	Lucero et al., 2020
HAM	3	A1, 42	Order level and below level	B1	Moss, unknown	Liu et al., 2014
CesA	26	A4, 46	Order level and below level	B1	Charophyta, unknown	Guo et al., 2016
FT/TFLl	6	A1, Unknown	Order level and below level	B1	Charophyta, MFT-like	Forero and Cvrckova, 2019
Myo	17	A1, 12	Order level and below level	B0	Charophyta, myo-xi (a)	Cao et al., 2017
NSR/RBP	2	A5, 7	Species level	B1	Unknown	Hussain et al., 2020
Cyc	50	A1, 10	Order level and below level	B1	Chlorophyta, unknown	Ifuku et al., 2008
OFP	19	A1, 19	Species level	B1	Moss, unknown	Jin et al., 2021
AQP	35	A1, 24	Order level and below level	B1	Chlorophyta, lips	Peremyslov et al., 2011
DLC	6	A1, 15	Order level and below level	B1	Chlorophyta, DLC-VIII	Boscolo-Galazzo et al., 2021
PsbP	2	Unknown	Unknown	B0	Unknown	Little et al., 2018
Signal transduction
CBL/CIPK	14/35	A2, 18	Order level and below level	B1	Unknown	Xiao et al., 2017
CDPK/CRK	34/8	A3, 6	Family level	B1	Unknown	Cao and Shi, 2012
GPAT	10	A1, 39	Order level and below level	B1	Chlorophyta, GPAT and GPAT9	Karlgren et al., 2011
PEBP	6	A3, 106	Order level and below level	B1	Unknown	Hedman et al., 2009; Zhang X. X. et al., 2020
RALF	33	A4, 4	Family level	B1	Unknown	Finet et al., 2013
ARF	23	A2, 21	Unknown	B0	Unknown	Saand et al., 2015
CNGC	20	A4, 15	Unknown	B0	Unknown	Ogilvie et al., 2014
CEP	12	A3, 106	Order level and below level	B1	Unknown	Gallie and Liu, 2014
PAB	8	A1, 54	Unknown	B1	Unknown	Geng et al., 2021
Supply of nutrients or ions
VIT	6	A1, 14	Angiosperms	B0	Unknown	Strozycki et al., 2010
Fer	4	A0, 16	Order level and below level	B0	Unknown	Zhang Y. M. et al., 2020
VP	3	A0, 27	Order level and below level	B1	Rhodoplantae and Chlorophyta, unknown	He et al., 2013
PHO	9	A1, 32	Order level and below level	B1	Chlorophyta, unknown	Geng et al., 2021
CIMS	3	A1, 35	Species level	B1	Chlorophyta, unknown	Cao, 2019
Hydrolases
BAM	10	A0, 136	Order level and below level	B1	Unknown	Rody and de Oliveira, 2018
SUS	6	A4, 16	Species level	B1	Unknown	Thalmann et al., 2019
Other components
HMT	3	A2, 29	Unknown	B0	Unknown	Xu et al., 2019
FBP	211	A1, 34	Order level and below level	B1	Chlorophyta, unknown	Zhao et al., 2018

A0, Archaeplastida populations; A1, green plant population; A2, land plant population; A3, seed plant population; A4, angiosperm population; A5, dicotyledonous plant population. For the contributions made to the genome-wide repeat events (such as paleopolyploidization and WGD), B0 indicates that no effect was observed or had been studied, and BN indicates an effect caused by N repeats. The copy event refers to the level of replication events that impact copy number.

FIGURE 3.

Origin and expansion of plant gene families. Gene families in boxes representing their origin in green algae or earlier. Families include OPR (12-oxo-phytodienoate acid reductase), KCS (3-ketoacyl-coa synthase), AGO (Argonaute), TLP (thaumatin-like protein), NBS-LRR (nucleotide binding site leucine-rich repeat), ALOG (Arabidopsis LSH1 and Oryza G1), WOX (WUSCHEL-related), C3HDZ (class III homeodomain-zinc finger protein), 3R-MYB, PFDN (prefoldin), AOX (alternative oxidase), SH3P (SH3 and BAR domain-containing protein), CesA (cellulose synthase), FT/TFL1 (flowering locus t/terminal flower 1), Myo (myosin), Cyc (cyclin), AQP (aquaporins), DLC (dynein light chain), GPAT (glycerol-3-phosphate acyltransferase), VP (vacuolar-type H+-pyrophosphatase), PHO (phosphate 1), CIMS (cobalamin-independent methionine synthase), and FBP (F-box). Gene families listed in the star may have contributed to the development of Streptophyte algae or functional innovations in the plant community, and include AHL (AT-hook motif nuclear localized), HMGR (3-hydroxy-3-methylglutaryl coenzyme A reductase), Aux/IAA (auxin/indole acetic acid and auxin response factor), HAM (hairy meristem), and OFP (OVATE family protein).

Natural selection often drives the evolution of disease resistance-related genes to establish functional differentiation between these genes, with various external hazards leading to the vast expansion of the genes. For example, there are many structural variations in the leucine-rich repeat receptor-like kinase (LRR-RLK) gene family (Man et al., 2020). The resistance I genes from the NBS-LRR superfamily originated from Chlorophyta (green algae) and were classified into five categories according to their structural characteristics [Chlorophyta: RNL; Charophyta: CNL; Embryophyta (land plants): TNL, HNL, and PNL] (Shao et al., 2019). NLR genes (CNL, TNL) are clearly classified as being found in Solanaceae species; however, their prevalence varies markedly, with few reported within the genome of tomato plants and many more in those of potatoes and peppers (Borrelli et al., 2018). Another example is offered by the evolution of the AGO gene family, which encodes proteins associated with antiviral activity. This family may have experienced 133–143 repeat events and 272–299 loss events, including five major repeats. Specifically, the differentiation of green algae may have formed four major branches (I: 1/10, II: 5, III: 4/6/8/9, IV: 2/3/7) of the AGO gene family (Singh et al., 2015). Similarly, the DRB gene family is divided into two branches based on differences in the number of double-stranded RNA binding motifs (dsRBM); the number of DRB proteins also varies among different species (Clavel et al., 2016). The plant RDR (RNA-dependent RNA enzyme) family originated from copies of three monophyletic genes, RDRα, RDRβ, and RDRγ, and was dependent on species divergence (Zong et al., 2009). Plant DCL (Dicer-like), however, followed the evolutionary traces of early plant evolution through independent replication, remodeling its RNA binding pocket in response to virus resistance (Mukherjee et al., 2013). Finally, expansion of the TLP gene family in green algae (1), mosses (6), and angiosperms (>20), may be based on tandem and segmental duplication events (Cao et al., 2016; Tables 1, 2; Figure 3).

Evolution of transcription factor gene families

Transcription factors function as regulatory elements of various plant processes, including growth, the stress response, and reproduction (Yang et al., 2008; Lian et al., 2014; Zhao et al., 2014; Finet et al., 2016; Vasco et al., 2016; Feng et al., 2017; Wu et al., 2017; Naramoto et al., 2020). Due to the rich evolutionary history of plants, TF gene families tend to have more members and a higher degree of functional differentiation compared with structural protein-related coding genes (Finet et al., 2016). In particular, the AHL gene family, which is related to plant growth and development, may have evolved from the fusion of algal PPC structural proteins and AT-hook motifs, and is thought to have originated in bryophytes. This family can be divided into three groups (A: I; B: II, III), with a high degree of gene loss and numerous duplication events throughout evolution (Zhao et al., 2014). The WOX gene family, which is involved in cell division, originated in green algae and is primarily divided into nine classes (WOX1/2, WOX5/7, WOX3, WOX4, WOX6, WOX11/12, WOX13, and WUS) with WOX13 being recognized as the oldest branch. Indeed, WOX genes exhibit significant variation in their motifs and number of members throughout their evolutionary process (Lian et al., 2014). CPP-like genes, which are associated with plant development, are divided into four branches: Gene deletion and species-specific amplification have been important in expanding this gene family, while positive selection has served as the primary evolutionary driving force (Yang et al., 2008).

The SPL/SBP family mainly includes nine subbranches, among which there are obvious evolutionary differences; their formation may be completed before the differentiation of the angiosperms (Preston and Hileman, 2013). The nine evolutionary branches, namely, SPL evolutionary branch-I, evolutionary branch-II, evolutionary branch-IV, evolutionary branch-V, evolutionary branch-VI, evolutionary branch-VII, evolutionary branch-VIII, and evolutionary branch-IX, are characterized by differences in function and altered mi RNA regulatory differences (Preston and Hileman, 2013). The TCP gene family consists of two main classes (classes I and II, i.e.: the CIN and CYC/TB1 evolutionary branches) (Liu et al., 2019). Among them, all land plants have CIN evolutionary branch TCP genes, while CYC evolutionary branch genes are only found in true dicotyledons and monocotyledons (Liu et al., 2019). In addition, the rapid expansion of the TCP gene family is consistent with a polyploidy trend in land plants, with fewer tandem duplication events (Liu et al., 2019). 3R-MYB is a regulatory TF associated with drought-resistance and development. Its structure is progressively more complex in different species groups, in conjunction with a gradual increase in the number of gene family members, forming three branches (A, B, and C3) in angiosperms (Feng et al., 2017). The family of ALOG genes, which regulate reproductive growth, originated in green algae and expanded significantly in angiosperms (Naramoto et al., 2020). The YABBY and C3HDZ gene families, associated with leaf growth, have evolved in stages of biological evolution and their molecular structures have given rise to several major branches with different molecular classes exerting unique effects on leaf development (Finet et al., 2016; Vasco et al., 2016).

Moreover, the MADS and AUX/IAA gene families originated in early land plants (mosses) and expanded to encompass multiple gene sub-family classes that have shown rich functional differentiation with multiple rounds of evolutionary events (Theissen et al., 2016; Wu et al., 2017). Specifically, the MADS domains in plants originated from the transformation of topoisomerase IIA subunit A (TOPOIIA-A) into MRCA and the latter’s subsequent modification to SRF-like and MEF2-like MADS-box genes. Furthermore, in angiosperms, type II MADS-box genes mediate major evolutionary innovations in plant flowers, ovules and fruits, whereas the formation of the Mγ and interacting Mα genes (Mα*) of type I MADS-box can be traced back to the angiosperm ancestor and may be related to its heterodimeric function in angiosperm-specific embryonic trophoblast endosperm tissue (Qiu and Claudia, 2021). This evolutionary process was affected by various events, including replication and functional differentiation, resulting in the functional diversity of their regulatory properties (Ng and Yanofsky, 2001; Gramzow et al., 2010; Airoldi and Davies, 2012; Theissen et al., 2016; Schilling et al., 2020; Hsu et al., 2021; Tables 1, 2; Figure 3).

Evolution of metabolic enzyme gene families

Metabolites are a direct manifestation of plant physiology. Highly specific biochemical processes that produce various metabolites have driven the formation and functional specialization of metabolic gene clusters (Duplais et al., 2020). Studies investigating the recurring events that led to the development of plant metabolic enzyme gene clusters have revealed a close relationship among the different metabolites (Duplais et al., 2020). The CYP/P450 gene family of mono-oxygenases is highly abundant in angiosperms, possibly due to multiple repeated events (polyploidy, tandem replication, and fragment repeat). They can be divided into two categories, A-type (e.g., CYP71) and non-A-type (e.g., CYP51, CYP72, CYP74, CYP85, CYP86, CYP97, CYP710, CYP711, CYP727, and CYP746), with CYP51 and CYP97 potentially representing the oldest clades (Su et al., 2021). The ACO gene families associated with respiration were almost lost early in the evolutionary path; however, they subsequently expanded and currently exist as large, functionally distinct subclasses (Wang et al., 2016; Tables 1, 2; Figure 3).

The OPR gene family of jasmonic acid biosynthesis-related enzymes doubled in number during the evolution of algae to land plants and further expanded via polyploidization and tandem duplication events. This gene family comprises seven categories. All OPR genes from green algae form subclade VII, subclade VI (present only in lower land plants), and subclade II (present in all land plants except the gymnosperm Picea sitchensis); subclade I is composed of gymnosperm and angiosperm sequences. Only monocotyledon sequences comprise subbranches III, IV, and V. The OPR gene family is particularly abundant in rice and sorghum (13 genes) (Li et al., 2009).

The HMGR gene family is associated with terpene biosynthesis and originated from bryophytes. It has only expanded in maize, soybean, cotton, and poplar, with each species containing five HMGR genes (sporophyte-specific branch, monocotyledon-specific branch HMGR III/IV, and dicotyledon-specific branch HMGR I/II) with different conserved sequences (Li et al., 2014).

The KCS gene family, which is involved in ultra-long-chain fatty acid synthesis, is divided into five main sub-clades (A, B, C, D, and E) with the number of genes in this family gradually increasing from one in algae to eleven in angiosperms, and with an apparent trend in the expansion of related polyploid species (Little et al., 2018).

Evolution of protein families associated with plant cell structure

Proteins with roles in cell wall formation and other aspects of cell structure are important for plant morphogenesis and can have basic enzymatic reactions. These proteins tend to have a low probability of gene loss, but they can accumulate a high degree of functional differentiation throughout a long evolutionary process, as observed within the CesA family of cellulose synthases (Little et al., 2018). The PSBP gene, encoding the light-harvesting protein complex PSII, only exists in the green plants of polymorphic biological groups that consist of few members with obvious structural differences (Ifuku et al., 2008). Cell cycle-related Cyc genes are divided into ten branches, most of which existed before green algae and became widely expanded during the transition to angiosperms (Boscolo-Galazzo et al., 2021). DLC genes associated with the dynein system are derived from DLC-VIII genes of green algae. With the gradual expansion of DLC genes along the evolutionary path, each plant type produced unique molecules (e.g., algae: DLC-VIII, bryophyte: DLC-VII, fern: DLC-IV, monocotyledon: DLC-I/II, dicotyledon: II/V), with a common branch in seed plants (DLC-VI) (Cao et al., 2017). The actin-associated Myo gene produces Myo-XI (A) in green algae and gradually extends into ten branches (Peremyslov et al., 2011). The aquaporin-encoding gene AQP developed from the LIPS type gene in green algae and gradually diverged into eight significantly different AQP genes (GIPS, LIPS, HIPS, XIPS, SIPS, PIPS, TIPS, and NIPS) in various plants, including soybean, upland cotton, and oilseed rape (Hussain et al., 2020). The RNA splice component NSR/RBP was slightly extended in soybean but contained differences in its conserved motifs (Lucero et al., 2020; Tables 1, 2; Figure 3).

The SH3P gene family, associated with cell plate formation, may have originated from the SH3P1-like ancestor of Charophyta and gradually expanded during the transition to mosses and angiosperms (Forero and Cvrckova, 2019). The cellulose synthase superfamily CesA, associated with cell wall formation, developed several branches among different species (CSLA and its developed branches CSLC and CESA, CSLB/H and its developed branches CSLF, CSLJ/M, CSLG, and CSLE). Moreover, the different subfamilies exhibit obvious selection for sugar synthesis. For example, certain members of the CSLJ subfamily may mediate (1, 3;1, 4)-β-glucan biosynthesis (Little et al., 2018). The FT/TFLL gene family, associated with flowering time, developed from MFT-like in angiosperms and contains several members (6) (Jin et al., 2021). The OFP gene family, associated with fruit shape, may have originated from the ancestors of land plants. Different species have varying numbers of these genes, which have been divided into 11 classes, due to numerous copy-number loss events (Liu et al., 2014). HAM gene families associated with tissue formation were generated from bryophytes and exhibit several molecular differences among different plant classes, where each family formed one branch. These gene families expanded in seed plants and ultimately evolved into two angiosperm branches (Type-I and Type-II) (Geng et al., 2021; Tables 1, 2; Figure 3).

Evolution of signal transduction gene families

Studies on signal transduction-related gene families showed that the number of PAB gene families, which are involved in promoting mRNA stability and protein translation, varies significantly among different groups. These gene families are divided into three groups (Class I: PAB1/PAB3/PAB5, Class II: PAB2/PAB4/PAB8, and Class III: PAB6/PAB7); however, their individual evolutionary routes remain unknown (Gallie and Liu, 2014). In seed plants, small peptide signal-related CEP gene families may have significantly expanded via WGD, especially in the Gramineae and Solanaceae (Ogilvie et al., 2014). The CNGC gene family, which act in calcium-gating, are divided into five classes (Groups I, II, III, IVA, and IVB), and the number of members within each class varies considerably (Saand et al., 2015). Auxin response factors are classified into three classes and seven groups (Class A: ARF5/7, ARF6/8; Class B: ARF1, ARF2, ARF3/4, ARF9; and Class C: ARF10/16/17) and were formed through the evolution of three bryophyte proteins (Finet et al., 2013). The alkalization factor RALF genes are divided into ten classes and may have developed from two primitive ancestors (Cao and Shi, 2012; Tables 1, 2; Figure 3).

The number of CBL, CIPK, CDPK, and CRK gene members associated with calcium signaling differs significantly across evolutionary stages (during the transition from lower plants to core angiosperms), and this phenomenon may be due to the abundant occurrence of WGD events and gene loss at these evolutionary stages. These polyploidy events then promoted the functional differentiation of corresponding proteins (Xiao et al., 2017; Zhang X. X. et al., 2020). Although only two PEBP genes, which are bind phospholipids and have roles in signal transduction, have been characterized in gymnosperms, they are particularly abundant in angiosperms, and their secondary expansion appears to be related to the formation of seed plants and angiosperms (Hedman et al., 2009; Karlgren et al., 2011). GPAT genes, which are associated with glycerol 3-phosphate biosynthesis, emerged earlier than those present in green algae, from which GPAT and GPAT9 developed into several GPAT genes in land plants (Waschburger et al., 2018; Tables 1, 2; Figure 3).

Evolution of other gene families

During evolution, other plant gene families have generated a high number of members with functional differentiation. In the salt or nutrient signaling pathways, the phosphorus transporter-encoding gene (PHO) contains obvious differences in copy number [from 0/1 when developed in green algae to two gradually more complex branches (C-1 and C-2) in land plants], protein structure, and number of introns (He et al., 2013). The ion transduction VP gene is divided into two branches, II and I, which originated from red algae and green algae, respectively. These branches were affected by polyploidy and were expanded in angiosperms (Zhang Y. M. et al., 2020). The plant ferritin Fer gene was already present in red algae and marginally increased in copy number in the later clades. Notably, the Fer gene of the monocotyledonous plant Lycoris aurea (Asparagales) appears more comparable to that of dicotyledonous plants (Strozycki et al., 2010). VIT genes encoding iron transporters consist of five ancient branches; however, two duplication events and six loss events led to substantial contraction of non-angiosperm VIT genes, and a subsequent expansion in copy number in angiosperms (Cao, 2019). Meanwhile, there is no significant difference in the number of methionine biosynthesis-related gene family (CIMS) members among green plants; however, multiple gene loss and gene duplication events occurred. In addition, WGT (wide-genome triploidy) led to the expansion of CIMS genes in soybean and alfalfa (Rody and de Oliveira, 2018; Tables 1, 2; Figure 3).

There has been obvious expansion and gene loss of the β-glucohydrolase (BAM) gene in different groups of hydrolases, which were divided into eight branches (Bam1, Bam10, Bam3, Bam4, Bam9, Bam5/6, Bam2/7, and Bam8) that existed before the formation of land plants. However, significant gene losses have occurred in basal land plants (Thalmann et al., 2019). The SUS gene family, which is involved in glycolysis, can be divided into three groups containing members that may have developed from WGD and that have also undergone obvious expansion in certain higher plants (Xu et al., 2019). Among the genes related to epigenetic factors, the methylation-related HMT family has two branches (Class 1 and Class 2) in land plants, especially in seed plants, indicating that the HMT genes underwent two separate functional differentiation events (Zhao et al., 2018). The ubiquitin-related FBP family that originated in green algae has undergone significant expansion in lower plants, monocotyledons, and dicotyledons, such as Brassicaceae (Navarro-Quezada et al., 2013; Tables 1, 2; Figure 3).

Concluding remarks and perspectives

Although it is desirable to develop better plant-based products and improve plant stress resistance for commercial reasons, it can be challenging to decipher the molecular profiles of plants and efficiently generate molecular resources (Nelson and Werck-Reichhart, 2011; Zhang et al., 2019). The development of plant molecular biology techniques has enabled the key events in plant evolution to be systematically characterized, including the molecular mechanisms underlying the adaptation of plants to life on land and plant hybrid formation (Cheng et al., 2019; Wang et al., 2021). To adequately assess the molecular evolution of plants, it is necessary to investigate a large variety of plant gene families. In particular, it is critical to analyze the unique features of the origin and evolutionary branches of different gene families.

The evidence described in this review suggests that gene duplication and gene loss occurred in nearly all gene families during plant evolution. Genes encoding TFs, proteins involved in disease and stress resistance, structural proteins, and signal transduction-related proteins have been extensively studied compared to genes in the hydrolase gene family (Shao et al., 2019; Lucero et al., 2020; Jin et al., 2021). Moreover, most research on molecular evolution has employed a small number of species and lacks systematics analysis. Therefore, it is necessary to conduct large-scale evolutionary studies on a broader selection of species groups, as well as the evolution of other functional genes, such as those encoding RNA-modifying proteins and autophagy-associated proteins.

Considering the content of these related studies, we believe that the following three aspects can be explored in the future to promote the understanding of plant molecular evolution-related processes. (A) the subfunctionalization of large families and the systematic evolutionary patterns of signaling pathways; (B) the comprehensiveness of the selection of representative plant taxa in molecular evolution studies and the statistical determination of related properties; (C) the origin of families, especially gene families associated with specific evolutionary events.

In summary, we have reviewed the molecular evolution of plants and discussed the potential contributions, challenges, and strategies associated with the gene families involved in the molecular evolution of plants as plants adapted to terrestrial environments and developed resistance to stress. The formation of different plant taxonomic units is closely associated with various plant gene families and their subsequent changes, most of which are characterized by traits that promote their environmental adaptability (Cheng et al., 2019; Shao et al., 2019; Man et al., 2020; Schilling et al., 2020). The transition of basal plants, such as Spiragloeophycidae and Streptophyte algae, often involved elaborate mechanisms to enhance plant resistance to environmental stress. For example, differences in the degree of water dependence and oxygen use occurred during the adaptation of plants for terrestrial environments. Investigation into relevant molecules, such as proteins encoded by key genes associated with the plant transition to terrestrial environments, can provide a pathway to enhancing the natural resistance of plants, thereby reducing their dependence on environmental growth conditions, and improving crop yield (Cheng et al., 2019; Figure 3).

Author contributions

YF wrote the manuscript. XL, JJ, XH, JG, DZ, and XX completed the revision of the manuscript. All authors contributed to the article and approved the submitted version.

Funding

This research was funded by the National Natural Science Foundation of China (32060614), the Guizhou Provincial Science and Technology Project ([2022]091), the China Postdoctoral Science Foundation (2022MD713740), Department of Education of Guizhou Province (QianJiaoHe YJSKYJJ[2021]056), and Project of Serving the Country Industrial Revolution Strategic Action Plan of Regular Undergraduate Regular Higher Institutions in Guizhou Province (Qian Jiao He KY Zi [2018] 093).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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