Science, Irving K. Barber Faculty of (Okanagan)
Non UBC
Biology, Department of (Okanagan)
DSpace
Agronomy 12 (10): 2582 (2022)
Luo, Qing
Meng, Ping-Hong
Jiang, Da-Wei
Han, Zhong-Ming
Wang, Zhen-Hui
Tan, Guo-Fei
Zhang, Jian (Professor of biology)
Houttuynia cordata Thunb., called Yuxingcao in Chinese, is an important medicinal plant and vegetable consumed in the southern regions of China. This review aims to summarize studies on the phyto-physiological chemistry, cytology, molecular biology, and genomics of H. cordata. Studies on the physiology and biochemistry of H. cordata have grown over the past few decades. Phenotypic and agronomic traits, tissue culture, elemental analysis, photosynthetic studies, bioactive compound identification, and antioxidant research have been reported. Molecular biological studies, such as those of molecular markers, microRNAs, DNA variations, protein variations, and transcriptomes have also advanced. Recent studies have focused on the rDNA and chloroplast genome of this plant. This review could serve as a basis to perform the genetic breeding, genomic advance, and cultivation of this valuable diversified plant resource for medicinal applications and vegetable production.
Citation: Luo, Q.; Meng, P.-H.; Jiang,D.-W.; Han, Z.-M.; Wang, Z.-H.; Tan,G.-F.; Zhang, J. ComprehensiveAssessment of Houttuynia cordataThunb., an Important MedicinalPlant and Vegetable. Agronomy 2022,12, 2582. https://doi.org/10.3390/agronomy12102582Academic Editor:Ferdinando BrancaReceived: 28 August 2022Accepted: 17 October 2022Published: 20 October 2022Publisher’s Note: MDPI stays neutralwith regard to jurisdictional claims inpublished maps and institutional affil-iations.Copyright: © 2022 by the authors.Licensee MDPI, Basel, Switzerland.This article is an open access articledistributed under the terms andconditions of the Creative CommonsAttribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).agronomyReviewComprehensive Assessment of Houttuynia cordata Thunb.,an Important Medicinal Plant and VegetableQing Luo 1,2, Ping-Hong Meng 2, Da-Wei Jiang 3, Zhong-Ming Han 4, Zhen-Hui Wang 1 , Guo-Fei Tan 1,2,*and Jian Zhang 1,5,*1 Faculty of Agronomy, Jilin Agricultural University, Changchun 130118, China2 Institute of Horticulture, Guizhou Academy of Agricultural Sciences, Guiyang 550000, China3 College of Horticulture, Jilin Agricultural University, Changchun 130118, China4 College of Chinese Medicinal Materials, Jilin Agricultural University, Changchun 130118, China5 Department of Biology, University of British Columbia, Okanagan, Kelowna, BC V1V 1V7, Canada* Correspondence: tagfei@foxmail.com (G.-F.T.); jian.zhang@ubc.ca (J.Z.)Abstract: Houttuynia cordata Thunb., called Yuxingcao in Chinese, is an important medicinal plantand vegetable consumed in the southern regions of China. This review aims to summarize studies onthe phyto-physiological chemistry, cytology, molecular biology, and genomics of H. cordata. Studieson the physiology and biochemistry of H. cordata have grown over the past few decades. Phenotypicand agronomic traits, tissue culture, elemental analysis, photosynthetic studies, bioactive compoundidentification, and antioxidant research have been reported. Molecular biological studies, such asthose of molecular markers, microRNAs, DNA variations, protein variations, and transcriptomeshave also advanced. Recent studies have focused on the rDNA and chloroplast genome of this plant.This review could serve as a basis to perform the genetic breeding, genomic advance, and cultivationof this valuable diversified plant resource for medicinal applications and vegetable production.Keywords: H. cordata Thunb.; phyto-physiological chemistry; molecular biology; genome; gene1. IntroductionHouttuynia cordata Thunb., also called Yuxingcao in China (Figure 1), is the solespecies in the genus Houttuynia of the family Saururaceae, which consists of the genera ofSaururus (S. chinensis and S. cernus), Gymnotheca (G. involucrate and G. chinensis), Anemopsis(A. californica), and Houttuynia (H. cordata); however, the species of A. californica and S. cernusare not found in China [1–4]. H. cordata is a perennial, polyploid (diploid or tetraploid)flowering herb native to China, Japan, Korea, northeast India, and Southeast Asia [5,6]).The predominant chromosome of H. cordata is X = 9 (2n = 18~108). It is distributed inthe central, southeastern, and southwestern regions of China. Some scholars speculatedthat it originated in the southwest of China. It was then transplanted and formed threegroups [4,7,8]. This plant grows well in moist to soggy soil, on shady hillsides, waysides,and ridges of fields with an altitude of 300~2600 m, produces a unique fishy smell, andblooms white flowers in early summer [9–11]. Interestingly, this herb propagates throughthe formation and separation of underground stems and parthenogenesis rather than sexualreproduction [12].As a common aromatic, medicinal, and vegetable plant, H. cordata is an important herbplant resource to the food, pharmaceutical, and aromatic industries. It has great value in thefields of ethnopharmacology, fermented products, and natural products chemistry [13–15].It has been traditionally used as a therapeutic plant in folk medicine during the last century,and its phytochemical ingredients (such as essential oils, alkaloids, organic acids, fattyacids, sterols, amino acids, and microelements) are used in some pharmaceutical formulas.It has been applied to treat various diseases because of its pharmacological functions,Agronomy 2022, 12, 2582. https://doi.org/10.3390/agronomy12102582 https://www.mdpi.com/journal/agronomyAgronomy 2022, 12, 2582 2 of 18such as diuretic, anti-microbial, anti-viral, anti-cancer/anti-tumor, anti-inflammatory, anti-oxidative, anti-diabetic, anti-allergic, and anti-mutagenic effects [16–21].Agronomy 2022, 12, x FOR PEER REVIEW 2 of 16 Figure 1. Morphological characteristics and utilization of H. cordata. (A). Wild H. cordata; (B). Above ground and underground part of H. cordata; (C). Flower and leaves of H. cordata; (D). Cultivated H. cordata; (E). Harvested H. cordata; (F). H. cordata above ground part used for medicinal material; (G,H). H. cordata roots as vegetable; (I). Fresh roots used for salad. As a common aromatic, medicinal, and vegetable plant, H. cordata is an important herb plant resource to the food, pharmaceutical, and aromatic industries. It has great value in the fields of ethnopharmacology, fermented products, and natural products chemistry [13–15]. It has been traditionally used as a therapeutic plant in folk medicine during the last century, and its phytochemical ingredients (such as essential oils, alka-loids, organic acids, fatty acids, sterols, amino acids, and microelements) are used in some pharmaceutical formulas. It has been applied to treat various diseases because of its pharmacological functions, such as diuretic, anti-microbial, anti-viral, an-ti-cancer/anti-tumor, anti-inflammatory, anti-oxidative, anti-diabetic, anti-allergic, and anti-mutagenic effects [16–21]. However, limited information has been obtained on the germplasm resources, from phenotypic diversity to heritable variation in H. cordata. Thus, this review aims to sum-marize studies on the phyto-physiological chemistry, cytology, molecular biology, and genomics of H. cordata. Hopefully, this review could provide some usefultheoretical and practical information to assist breeding research of H. cordata. Further studies are war-ranted to obtain further information, including the genomics, of H. Cordata. 2. Physiology and Biochemistry 2.1. Phenotypic Diversity and Agronomic Traits Previous studies have described and classified morphologies of the leaves, stems, flowers, and rhizomes of H. cordata. The geo-herbalism of H. cordata is largely deter-Figure 1. Morphological characteristics and utilization of H. cordata. (A). Wild H. cordata; (B). Aboveground and underground part of H. cordata; (C). Flower and leaves of H. cordata; (D). CultivatedH. cordata; (E). Harvested H. cordata; (F). H. cordata above ground part used for medicinal material;(G,H). H. cordata roots as vegetable; (I). Fresh roots used for salad.However, limited information has bee obtained on the germplasm resources, fromphenotypic diversity to ritable variation in H. cord ta. Thus, th s review a ms to sum-marize studies on the p yt -physiological chemistry, cytology, molecular biology, andgenomics of H. cordata. Hopefully, this review could provide some usefultheoretical andpractical information to assist breeding research of H. cordata. Further studies are warrantedto obtain further information, including the genomics, of H. Cordata.2. Physiology and Biochemistry2.1. Phenotypic Diversity and Agronomic TraitsPrevious studies have described and classified morphologies of the leaves, stems,flowers, and rhizomes of H. cordata. The geo-herbalism of H. cordata is largely determinedby its genetic factors, which have been used to guide the cultivation, breeding, and tiliza-tion of wil H. cordata populations [22–24]. Guan (2010) analyzed the genetic variation inmorphological characteristics of 20 H. cordata germplasm populations, and the populationswere divided into 3 groups through cluster grouping with 15 measurable traits, showing aAgronomy 2022, 12, 2582 3 of 18rich variation among these populations [25]. Shun et al. (2014) analyzed and showed thatenvironmental factors exert different effects on the formation and accumulation of activephysiochemical compounds in H. cordata [26]. Li et al. (2018a) analyzed the phenotypicdiversity of leaf traits (9 phenotypic traits and 6 relative traits) in cultivated H. cordata pop-ulations from Hunan province in China, and showed that the diversity of leaf phenotypictraits is mainly determined by genetic factors, providing a theoretical basis for the breedingof excellent germplasms [27].2.2. Elemental AnalysisH. cordata is a vegetable rich in proteins, minerals, vitamins, and amino acids, givingH. cordata its high nutritional and economic value [28,29]. Many studies analyzed theelemental composition of H. cordata. Qin and Yang (2015) measured the contents of 5 traceelements (calcium: Ca, magnesium: Mg, iron: Fe, zinc: Zn, and copper: Cu) through atomicabsorption spectrophotometry, and the results showed that the order of element content inthe same organ is Mg, Ca, Fe, Zn, and Cu [30]. Mo et al. (2015) compared the contents of10 macro-elements and micro-elements in the leaves, aerial stems, and underground stemsof wild H. cordata from different regions, and found that this plant is rich in sulphur (S),phosphorus (P), potassium (K), Ca and Mg [31]. Li et al. (2018b) detected the contents of14 heavy metals (manganese: Mn, Zn, Cu, cobalt: Co, titanium: Ti, stannum: Sn, antimony:Sb, barium: Ba, chromium: Cr, nickel: Ni, arsenic: As, plumbum: Pb, mercury: Hg andcadmium: Cd) in H. cordata via the inductively coupled ICP-MS (inductively coupled plasmamass spectrometry) method, and the results showed that the linear relationship betweenthe concentration of each element ranges from 0.15 to 695 g·L−1 [32]. Fotev et al. (2018)concluded that the micro-elements of H. cordata accumulated Mn, Fe, and Cu in the leaves,whereas Fe, Co, Cu, and Zn are detected mainly in the roots [11].2.3. Photosynthetic TranspirationThe photosynthetic transpiration of plants is directly related to their growth potentialand the economic benefits for farmers. Therefore, photosynthesis studies of H. cordata areimportant. Huang et al. (2006) measured the photosynthetic and transpiration charac-teristics of H. cordata, and found that photo flux quantum (PFD), relative humidity (RH),stomatal conductance (Gs), and leaf temperature (Tl) significantly correlate with the net-photosynthetic rate (Pn) and transpiration rate (Tr). PFD and Ca (air CO2 concentration) arethe major Pn-affecting factors, and PFD and Ta (air temperature) are the main Tr-affectingfactors [33]. Xu et al. (2011b) explored the optimal potassium concentration for the propergrowth and physiological response of H. cordata and found that 1.28 mM potassium is theoptimum concentration to obtain the optimal values of dry weight, shoot height, root lengthand number, H2O2 content, superoxide dismutase activity, and net photosynthetic rate [34].Lv et al. (2012) tested the effect of different concentrations of NaCl on the photosynthesis ofH. cordata at different habitats, and concluded that H. cordata from Huaihua County, HunanProvince showedimproved photosynthesis and adapt to salt stress [35].2.4. Effects of Bioactive Compounds onAntioxidantCapacitiesof H. cordataSome studies investigated the nutritional quality and health benefits, and other studiesanalyzed the bioactive substances and antioxidant capacity of different parts of H. cordata.Li et al. (2007) tested the effects of Pb, Zn, and their interactions on the chlorophyll contentand antioxidant enzyme systems of H. cordata and found that treatment with Pb or Znalone exerts more beneficial effects on chlorophyll content and antioxidant enzyme systemsthan their combination. It was also shown that H. cordata might have a high tolerance toPb [36]. Cai et al. (2013) analyzed the total phenol and flavonoid contents and antioxidantactivity of leaves from 16 H. cordata cultivars, showing that it isdivided into two types(I and II type) based on comprehensive agronomic characteristics. The total phenol andflavonoid contents and antioxidant activities of all materials were different due to theirgenetic backgrounds, in particular, the chromosome number (more than 80) of the materialAgronomy 2022, 12, 2582 4 of 18which had the highest total phenol and flavonoid contents and antioxidant activity [37].Wang et al. (2015) tested the effects of LED (lightemitting diode) light spectra on the activeoxygen metabolism and expression of antioxidant is ozymes in H. cordata seedlings and foundthat the antioxidant system of H. cordata seedlings is more sensitive to short light wavelengththan to long light wavelength [38]. Liu et al. (2016) analyzed the bioactive compounds andantioxidant capacities in H. cordata, and the results indicated that (1) the levels of carotenoids,chlorophyll, anthocyanins, vitamin C, pro-anthocyanidins, total phenolics, flavonoids, andantioxidantcontents can be arranged in the order ofleaves > stems > rhizomes; (2) asignificantpositive correlation exists between antioxidant capacities and seven bioactive compounds(p < 0.05); and (3) the leaves contain more bioactive compounds and anti-oxidant capacitythan the stems and rhizomes. Furthermore, a comparison with 8 types of common vegetablesrevealed that H. cordata has great potential for development because this plant, especiallyits leaves, contains more bioactive substances and higher antioxidant capacity than othervegetables [39].2.5. Bacteriostatic and Anti-Tumor/Anti-Cancer EffectsPrevious studies reported the anti-tumor and anti-microbial properties of H. cordata [40–42].Anti-microbial (including anti-bacterial, and anti-fungal) function is the most basic pharmaco-logical function of H. cordata, as has been established through long-term and in-depth studies [43].H. cordata extracts can effectively inhibit microorganisms, such as Staphylococcus aureus,Escherichia coli, Bacillus subtilis, Pseudomonas aeruginosa, Aspergillus niger, Bacillus polymyxa andSaccharomyces cerevisiae [44–47]. Secondary metabolites from Streptomyces sp. K15, an endophytein H. cordata, show anti-microbial activities, particular lyagainst Botrytiscinerea [48]. H. cordatacombined with other drugs (such as levofloxacin, and penicillin) exerts a germicidal actionagainst bacteria (such as S. aureus) with biological envelopes [49,50]. The endophytic fungusJ3, isolated from H. cordata and identified as Fusarium oxysporum, demonstrates anti-microbialactivities against S. aureus and Enterococcus faecalis [51]. Another endophytic fungus (Chaetomiumglobosum and F. oxysporum) was also identified to exhibit a good broad-spectrum bacteriostaticeffect [52,53].Some studies also focused on the anti-tumor/anti-cancer effects of H. cordata [54,55].H. cordata extract inhibits cell growth and induces apoptotic cell death in human primarycolorectal cancer cells through a mitochondria-dependent signaling pathway [56]. Theextract of H. cordata modulates G0/G1 phase arrest and Fas/CD95-dependent apoptoticcell death in human lung cancer A549 cells [57]. Meanwhile, extract of H. cordata inducesA375 programmed cell death in human melanoma cells by p38 phosphorylation asso-ciated with HMGB1 reduction and by activating the caspase-dependent pathway [58].Kim et al. (2017) demonstrated that H. cordata promotes the activation of HIF-1A–FOXO3and MEF2A pathways to induce apoptosis in human HepG2 hepatocellular carcinoma cells,indicating that this plant is a promising candidate for anti-tumor drug development [59].Lou et al. (2019) showed that H. cordata and its bioactive compound 2-undecanone cansignificantly suppress benzo(a)pyrene-induced lung tumorigenesis byactivating the Nrf2-HO-1/NQO-1 signaling pathway significantly [60].2.6. Physiochemical CompoundsMany researchers authenticated the ingredients and function of the physiochemicalcompounds, such as polyphenols, and analyzed the relationship between the contentsof flavonoids and their biological characteristics in H. cordata by using high-performanceliquid chromatography (HPLC) [61,62]. Wu et al. (2002a,2002b) analyzed the peroxidaseand esterase isozymes variations of the germplasm resources of H. cordata from SichuanProvince in China and found 6 types of peroxidase isozyme bands (each band type wascomposed of from 4 to 6 bands, with the number in the north being higher than that insouthern areas) and 10 types of esterase isozyme bands (each band type was composed offrom 4 to 8 bands which had no geographic differences) [63,64].Agronomy 2022, 12, 2582 5 of 18Wu et al. (2009c) analyzed the content variation of flavonoids, including hyperin,quercitrin, and quercetin in H. cordata from 22 provinces or geographic origins in Chinaand found thatthe levels of the three major flavonoids vary remarkably from differentprovinces, the contents of quercetin is not correlated with the geographic region, andconcentrations from the highest to the lowest were in leaves, stems, and rhizomes [65].Shun et al. (2014) concluded that appropriate shade treatment not only avoids the inhibitoryeffect of strong light on its growth, but also significantly increases the contents of activecomponents [26]. Li et al. (2015a) examined the contents of major nutrient components,including protein, soluble sugar, fat, volatile oils, and total flavonoids, and the compositionand contents of medicinal substances under field conditions and natural light at fullintensity, 40% intensity, and 20% intensity in H. cordata from sprouting to harvesting. Thisstudy showed that sufficient light is necessary when growing H. cordata as medicinaland functional food, but appropriate shading or intercropping is necessary when thecrop is grown as food [66]. Se (2015) detected the pharmacological volatiles emanatingfrom3 different parts of H. cordata (leaves, aerial stems, and underground stems) fromSouth Korea through fast gas chromatography–surface acoustic wave sensor (GC/SAM)and identified 16 compounds from the leaves (71.0%) and aerial stems (50.1%), includingthe monoterpenes β-myrcene, cis-ocimene, and decanal in underground stems (74.6%),and2-undecanone (1.3%) and lauraldehyde (3.5%) in leaves [67]. Zhang et al. (2018)determined the four main volatile components (4-terpenol, α-terpilenol, bornyl acetate,and methylnonylketone) of 47 H. cordata germplasm resources. They screened out thehigh content of the volatile components and provided a theoretical basis for aspecial typeof breeding [68]. Chen et al. (2004) studied the relationship between the essential oilconstituents and the chromosome number of H. cordata and found a tendency for thenumber of essential oil spots to increase with the chromosome number [69].2.7. Secretory TissuesFew studies focused on the roots, aerial stems, leaves, rhizomes, and other organs(such as secretory tissues), which greatly differ in anatomical structure among differentpopulations of H. cordata [28,70]. Lin et al. (2013) showed that many oil cells in the leaves,stems, and rhizomes of H. cordata are the storage sites of volatile oil [71]. Some researchalso showed the structural, componential, and functional characteristics of its secretorytissues in the floral and vegetative parts of H. cordata [72].3. Cytology3.1. EmbryologyAlthough some researchers have studied the embryology of Saururaceae [73–75], stud-ies on the sexual reproduction of H. cordata are not comprehensive. In particular, previousstudies were insufficient for helping cross-breeding attempts [76]. Nuclear extrusion andabnormal meiosis possibly lead to the high pollen abortion rate (99.6%) of H. cordata [25].Subsequently, Guan et al. (2012) observed the cytomixis and meiotic abnormalities duringmicrosporogenesis in two populations of H. cordata with different ploidy levels (2n = 38~96),and found the origin of the intraspecific polyploidy, and suggested that it might lead to alarge variation in chromosome numbers in this species [77]. Lin et al. (2011) worked onthe histochemistry of anther development in H. cordata, and results showed that (1) somestarches are distributed in the epidermis and endothelium; (2) plasmolysis in the tapetalcells occurs at the period of microspore mother cells; and (3) lipid accumulation in pollengrains is insufficient during anther development [78]. Li et al. (2010) reported that H. cordatapollen grains are abortive for deficiency of lipids in mature pollen grains [79]. Li et al. (2014)determined the pollen viability by I2-KI staining and examining the developmental courseof male and female gametophytes using paraffin sections, and the results showed that(1) H. cordata pollen viability is extremely low (3.18%); and (2) the male gametophyte isnormal in the early development stage and disintegrates in the dyad period of the tapetumcell. Then, the cytoplasm of free microspores gradually disappears and shows an emptyAgronomy 2022, 12, 2582 6 of 18flat shape, and the microspore shape changes from sub-orbicular to irregular. Finally,microspore abortion occurs before pollen sac cracking, which might lead to male sterility,and the seed might come from apomixes [80]. Li et al. (2017) reported that they are closelycorrelated with inflorescence size, anther color, and length at the meiosis stage, suggestingthat the uninuclear pollen development rather than the abnormal division of pollen mothercell meiosis is the main reason behind the low pollen counts in H. cordata [81].3.2. Intraspecific PolyploidyHsu (1967) studied the chromosomes of many vascular plants, including H. cordatafrom Taiwan, and suggested that the number of chromosomes of H. cordata is 24 [82]. Manyresearchers have studied the phylogenetic development of the Saururaceae plant, but theirconclusions were contradictory (Table 1).Agronomy 2022, 12, 2582 7 of 18Table 1. Analysis of the karyotype of H. cordata in different countries.Country Category Basic Number ofChromosomes ChromosomeNumber Scope Karyotype ReferencesChina G. chinensis Decne,G. involucrate Pei X = 9 2n = 18 [83]China H.cordata X = 9 2n = 36,54,72,81,126 36~126 [84]China 2n = 22 = 10 m + 10 sm + 2 t 2B [85]China Saururus L.,Houttuynia Thunb.X = 11,X = 122n = 22 = 4m + 16 sm + 2st,2n = 24 = 14 m + 10 sm [86]Eastern Asia (Nepal, China,northern Thailand, Taiwan,and Japan)X = 9,10,12 2n = 72,80,96,112,128 [87]China H. cordata X = 11,X = 122n = 20 = 14 m + 6 sm (Hefei,Wuhu) = 10 m + 10 sm (Anqing);2n = 22 = 14 m + 8sm (Chuzhou,Huoshan) = 18 m + 4sm(Huangshan);2 n = 24 = 16 m + 8sm (Chaohu)=18 m + 6sm (Tongling)=14 m + 10 sm (Jixi);2n = 26 = 16 m + 10 sm (Guangde);2n = 30 = 20 m + 10 sm (Shitai)=20 m + 10 sm (Neijiang);2n = 32 = 26 m + 6sm (Dujiangyan)=22 m + 10 sm (Luzhou)=18 m + 12 sm + 2 t (Zigong)20~32 1B,2B [88]China X = 8,9,12 2n = 108,99,94 (the highestfrequency),92,38,37,35 36~99 [25]The position of the centromere is expressed by the ratio of its long arm to its short arm. M: the ratio value is 1.0; m:the ratio value isfrom 1.0 to 1.7; sm: the ratio value is from 1.7 to 3.0;st: the ratio value isfrom 3.0 to 7.0; t: the ratio value is from 7.0 to ∞.Agronomy 2022, 12, 2582 8 of 184. Molecular Biology4.1. Molecular MarkerMany studies explored the genetics and taxonomy of H. cordata by using differentmolecular marker methods such as RAPD (polymerase chain reaction), SRAP (sequencerelated amplified polymorphism), ISSR (inter simple sequence repeat), and AFLP (ampli-fied fragment length polymorphism), and discussed the relationship among genuineness,genetic, and environmental factors [89–94]. Zhong et al. (2009) analyzed the differentiationcoefficients, genetic parameters, and diversity index on the population phenotypic traitsof 16 germplasm lines of H. cordata from Huaihua city of Hunan Province in China, andthe results showed that the differentiation coefficients are rich, and the differentiationdegrees are high in the populations [95]. Guan (2010) screened the collection of 34 H. cordatapopulations with SRAP primers and divided them into 3 groups based on the UPGMA(unweighted pair-group with arithmetic means) method, and the results suggested thatacorrelation exists between the genetic diversity and geographic distribution among theH. cordata populations [25]. Li et al. (2010) estimated the genetic diversity of differentgeographical populations of H. cordata from 13 provinces in China using AFLP markers andshowed that the coefficient of genetic distance is from 0.0089 to 0.1818 and that 15 popula-tions are grouped into 3 different clusters, suggesting the genetic diversity within differentgeographical populations of H. cordata in China is profound [79]. Zhong et al. (2011)analyzed the genetic characteristics of 16 H. cordata populations in Huaihua city of HunanProvince by SRAP markers, and the results divided 15 populations into 5 groups with agenetic distance of 0.5. No significant correlation was found between genetic structureand habitat factors; the gene differentiation coefficient and the gene flow increase withaltitude and decrease with increasing latitude and longitude [96]. ISSRs analysis revealedlow genetic variations within populations, and high genetic differentiations among pop-ulations. The structure of genetic diversity among 226 individuals from15 populationsof H. cordata in China suggests that this species might have survived in Southwest Chinaduring the glacial age, and subsequently experienced an eastern postglacial expansion [8].Wang’s (2010) conclusions also show that its phenotypic clustering and molecular clusteringare similar among different populations [92].4.2. microRNARecent studies have suggested that miRNAs play regulatory roles at the intracellularand intercellular levels, and even in the inter-species manner. He et al. (2019) identified163 conserved miRNAs and 30 novel miRNAs through high-throughput sequencing ofH. cordata and found that they are enriched in the endocrine and other factor-regulated Careabsorption pathways, the insulin signaling pathway, melanogenesis, and aldosterone-regulated sodium reabsorption pathways, via bioinformatics analysis on the targets ofH. cordata miRNAs to study the cross-kingdom functions of active compounds inH. cordata [97].4.3. DNA VariationDNA variation is the basis of the origin and diversity of species. Liu (2014) analyzedthe DNA variation of 46 strains of H. cordata from the same GAP (good agriculturalpractices) origin with ISSR and RAPD molecular markers through cluster analysis. Theresults showed that 9 ISSR primers and 8 RAPD primers have amplification of 134 and101 bands respectively, which helped to estimate the polymorphisms of the stripe numbers115 and 72 respectively. Additionally, polymorphic rates were 85.8% and 71.3% and theaverage genetic similarity (GS) coefficients were 0.6786 and 0.6947, respectively. Thisresult revealed that the gene possessed polymorphisms among H. cordata from the sameGAP area [62].Agronomy 2022, 12, 2582 9 of 184.4. Protein VariationSome studies have suggested that the stronger frost resistance of the plants located athigher altitudes is associated with their massive accumulation of protein, fat, starch, andrelated substances [98]. Liu (2014) has shown a wide range of protein types, with molecularweights ranging from 6.5 KD to 97.2 KD from the 53 lines of H. cordata, but the proteintypes warrant further clarification [62].4.5. TranscriptomeTo date, genomic information about H. cordata is still limited. Kim et al. (2010) per-formed the global transcriptome analysis of the E. coli O157 in response to the molecularmechanisms of H. cordata on its antibiotic effect [99]. Wei et al. (2014a) carried out thehigh-throughput transcriptomic sequencing of H. cordata to generate a large transcriptomesequence dataset, andtheir major findings are as follows: (1) over 56 million sequencingreads were produced from H. cordata mRNA by Illumina paired-end sequencing; (2) sub-sequent de novo assembly yielded 63,954 unigenes,39,982 (62.52%) and 26,122 (40.84%),of which 30,131 and 15,363 unigenes were assigned to gene ontology categories and clus-ters of orthologous groups, respectively; (3) 24,434 (38.21%) unigenes were mapped onto128 pathways and 17,964 (44.93%) unigenes showed homology to Vitis vinifera (Vitaceae)genes; and (4) 4800 cDNA (complementary DNA) SSRs were identified as potential molec-ular markers [100]. Li et al. (2016) analyzed the simple sequence repeats (SSR) loci informa-tion in the transcriptome of H. cordata contained 63,954 unigenes, and a total of 4800 SSRswere distributed in 4413 unigenes with adistribution frequency of 7.51%. Numerous SSRswith high frequencyand various types could provide the basis for studying the geneticdiversity and genetic map of H. cordata [101].5. Genome5.1. Plasmon Diversity (cpDNA and mtDNA)Some studies examined the chloroplast trnL-trnF and rps16 sequence variation ofthe alpine species Primula secundiflora. These studies revealed the phylogenetic structureof the distributed species in cpDNA (chloroplast DNA) [102]. Wu et al. (2005a) investi-gated the plasmon diversity of 70 H. cordata accessions by using PCR-RFLP and discussedthe phylogenetic relationship and phylogeographic information of the genus Houttuynia,and the results showed that 59 distinct organelle haplotypes could be identified among70 accessions, a total of 2 H. emeiensis and 57 H. cordata of the plasmon variations, theinterspecific and intraspecific relationships within the genus of Houttuynia, and the averageGSs values within H. emeiensis and H. cordata accessions, which reached 0.986 and 0.950,respectively [103].5.2. rDNASome researchers studied the intraspecific polymorphisms in the exon and group Iintron of subunit rDNA (ribosomalDNA) of the obligate plant parasite Plasmodiophora bras-sicae [104]. Zhao (2008) analyzed the nuclear ribosomal DNA based on internal transcribedspacer (ITS) sequences of 23 H. cordata germplasm resources from Sichuan province andChongqing city in China, including 11 cytotypes and 2 chemotypes, in total obtaining147 ITS sequences, and the PCR product length varied from 670 bp to 684 bp and the lengthof ITS1 varied from 231 bp to 245 bp, whereas that of ITS2 was uniformly 275 bp for allaccessions [105].5.3. Chloroplast GenomeAlthough the chloroplast genome contains many noncoding regions, relatively fewstudies focused on interspecific phylogenetic and intraspecific phylogeographic charac-teristics [106]. Yu et al. (2019) reported that the complete chloroplast genome sequence ofH. cordata is 161,090 bp in length, containing a large single copy (LSC) region of 88,180 bpand a small single copy (SSC) region of 19,204 bp, which were separated by a pair ofAgronomy 2022, 12, 2582 10 of 1826,853 bp inverted repeat regions, and H. cordata is a sister of Piper cenocladum [107].Zhu et al. (2020) carried out the de novo assembling of the complete chloroplast genomeof H. cordata and showed a typical quadripartite cycle of 160,226 bp, including a pairof inverted repeats (IRa and IRb) is 26,853 bp. It is separated by an SSC region of18,340 bp and an LSC region of 88,180 bp, including 112 unique genes, 79 protein codinggenes, 29 tRNA genes, and 4 rRNA genes. In addition, 81, 13, and 17 two copy geneswere located on the LSC, SSC, and IR region, respectively, and the chloroplast genome ofH. cordata (48 repeat sequences, 86 SSR motifs) had a close relationship with the Aristolochiaspecies (38~138 repeat sequences, from 95 to 156 SSR motifs), as revealed by mVISTAanalysis [108].6. Germplasm Genetic Resource6.1. Genetic DiversityIntra-species genetic variability assessment was used in formulating genetic im-provement and germplasm conservation strategy research. Wu et al. (2005b) tested thegenetic diversity of 70 H. cordata accessions from Sichuan, Chongqing, Guizhou, andJiangsu provinces in China by using RAMP, RAPD, and ISSR markers, and they arrivedat the following conclusions: (1) a higher degree of genetic diversity exists among thegermplasm resources of the genus Houttuynia at the molecular level (RAMP markers) [109],(2) the groups based on ISSR GS studies had been correlated with the same chromosomenumbers which could have been classified together, while correlated with geographicdistribution by RAPD GS [110].Wei and Wu (2012) assessed the level and distribution ofgenetic diversity in 226 individuals from 15 populations of H. cordata in China by usingISSR markers and revealed low genetic variations within populations, but high geneticdifferentiations among populations [8]. Gupta and Bharalee (2020) also assessed the geneticdiversity of H. cordata from four regions of northeast India, which contained 545 genotypesfrom 18 populations, and found that the genetic differentiation among 18 populations ishigh (Fst = 0.3894; p <0.001) with relatively restricted gene flow (Nm = 0.6564), whichsuggested that ex situ conservation could be an appropriate measure to adequately capturethe total genetic diversity of H. cordata populations in northeast India [111].6.2. GS Values of CytotypesStudies of the GS values of cytotypes provided the theoretical basis and the depthof research in another aspect of system diversity of H. cordata populations. Wu et al.(2002a) detected the genetic diversity of 92 H. cordata germplasm resources and found thatthe average GSs are from 0.52 to 0.572. Meanwhile, the interspecific GS is 0.517 amongthese 92 lines’ populations. All materials had been divided into 11 types. In addition,the same number of chromosomes tended to cluster together, while the groups classifiedaccording to the RAMP GS coefficient were related to the geographic distribution [62].Wu et al. (2003a) analyzed the genetic diversity of germplasm resources of H. cordataby ISSR marker and found that the chromosome number of 36 of H. cordata is the mostsimilar in their cellular types. The average value of their GS factors is 0.618. As such, greatgenetic deference certainly exists at the cellular level in the germplasm resources of H.cordata, but the medicinal compositions are determined by its genetic factors [112]. Wu et al.(2005b) showed that the GS between the accessions within H. emeiensis and H. cordata are0.660 and 0.575, respectively. Meanwhile, the GS value with the chromosome number of36 is 0.559 [109]. Zhao (2008) studied the cytotypes of 23 H. cordata materials containing A,B, C, D, E, F, G, H, I, J, and K, and the average tracytotypic GS values are 0.0056, 0.0040,0.0096, 0.0077, 0.0091, 0.0137, 0.0092, 0.0069, 0.0093, 0.0058, and 0.0089 respectively (withthe average of 0.0082).Of these, the GS of cytotypes F (chromosome number of 82) is thehighest (0.0137), (chromosome number of 72) is the medium (0.0096), and cytotypes B(chromosome number of 54) is the lowest [105].Agronomy 2022, 12, 2582 11 of 186.3. Gene Function CharacterizationIn recent years, cloning and studying the genetic functions of medicinal plants havebecome research hotspots. Thus, some studies focused on these aspects in H. cordata(Table 2). Furthermore, organic H. cordata harbors higher abundance and diversity ofanti-bacterial resistance genes (ARGs) than that of non-organic origin, but the ARGs arestill unknown [113].Agronomy 2022, 12, 2582 12 of 18Table 2. Cloning and studiesof gene function in H. cordata.Name Open ReadingFrame (ORF, bp)TransmembraneRegions Signal Peptide Motif DomainMolecularFormulaRelativeMolecularWeightIsoelectricPoint (PI)TranscriptAbundance ReferencesCHS1 1188 no two CHS C1920H3067N531O566S1743,190.7 6.38 Flowers>stems>rhizomes>leaves [114]DXS1 2172 no no DXS C3443H5456N958O1022S3577,745.1 6.57 Flowers>leaves>rhizomes>stems [115]DXR 1416 no no DXR C2298H3668N624O 671S1851,351.2 6.33 Leaves>rhizomes>stems>flowers [116]UGT75C1 1461 no no PSPG C2373H3740N638O714S1753,176.6 5.22 Leaves>stems>rhizome>flowers [117]AACT 1218 no no no C1812H2952N514O563S1941,555.6 6.13 Stems>rhizomes>flowers>leaves [118]HMGR 1626 two no HMGRNADPHC2565H4093N701O758S3057,841.7 7.10 Flowers>leaves>stems>rhizomes [90,119]Agronomy 2022, 12, 2582 13 of 186.4. Vegetativeand Sexual Production of H. cordataThe seed viability of H. cordata is lacking, and vegetative proliferation during winteris poor. Furthermore, H. cordata seeds are light-sensitive and small, with a low germi-nation rate [120,121]. Therefore, tissue culture techniques have been used for the rapidpropagation and conservation of elite clones of H. cordata throughout the years [122,123].Moreover, studies about the embryo sac, embryo, and the low pollen fertility of H. cordataare rarely reported, and the mechanism of male sterility was not studied [124]. Wang (2013)suggested the following:(1) the stigma pollen is incompatible with self-pollination andcross-pollination in the populations, stigma papilla cells produce callose, or the fertilitypollen grains germinate regularly but the pollen tube could not grow into the stigma,whereas the tapetum cells degenerate normally providing nutrition for microspore devel-opment; (2) the embryo sac development of H. cordata belongs to a monospore polygonumtype; and (3) during embryonic development, starch gradually accumulates in nucellarcells, resulting in nucellar cells of mature seeds filled with starch grains. Therefore, stempropagation is the main method of reproduction in the practical production culture ofH. cordata [125].6.5. Transgenic EngineeringIn recent years, molecular biology and genomic studies of H. cordata had been re-ported because of their research and economic value. Attempts to use H. cordata fortransgenic engineering as a model plant have been carried out. Lai (2008) studied theAgrobacterium tumefaciens-mediated cecropin foreign gene transfer in H. cordata, which pro-vided a theory for the anti-bacterial peptide expression in Chinese medicinal plants. Anti-microbial peptides are small molecules with broad-spectrum anti-microbial activity. Thesemolecules have become research hotspots of disease resistance breeding in plant geneticengineering. They are expressed in many plants with enhanced disease resistance [126].Dong et al. (2010a) transformed the anti-microbial fusion gene of peptides cecropinB andrabbit NP-1(CN) fused into H. cordata; this study showed that the fusion gene is expressedin the transgenic genome of H. cordata and that the transgenic plants show enhanced anti-bacterial ability [127]. Dong et al. (2010b) developed an Agrobacterium-mediated methodofgenetic transformation of H. cordata and integrated foreign DNA into the genome oftransgenic plants by using PCR and PCR-Southern analyses [128].7. ConclusionsH. cordata is an important medicinal plant and vegetable. At present, genetic diversity,and GS intra-species and inter-species of H. cordata have become increasingly valuable,and comprehensive utilization of germplasm resources remains to be conducted. Datamining and utilization of genome information of H. cordata can be applied to fill thisgap. These studies on pharmacology, cultivation, and breeding are equally important. Inaddition, the true value of H. cordata secondary metabolites should be considered [129,130].Obviously, it holds great research value, not only in medicine but also in agriculturalbiodiversity. In-depth research, however, still needs to be carried out in the molecular,breeding, physiological, genetic, and genomics fields to understand H. cordata.Author Contributions: Q.L., J.Z. and G.-F.T. conceived and designed the manuscript; G.-F.T., Q.L.,P.-H.M., D.-W.J., Z.-H.W. and Z.-M.H. analyzed the data; Q.L. and G.-F.T. wrote the paper; G.-F.T.,P.-H.M. and J.Z. revised the paper. All authors have read and agreed to the published version ofthe manuscript.Funding: This study was financially supported by the Guizhou Academy of Agricultural Sci-ences Project (QiannongKeyuan Support (2021) 05; Germplasm Resources of Guizhou Academy ofAgricultural Sciences No. (2020) 10); the Jilin Agricultural University high-level researcher grant523 (JLAUHLRG20102006); the Vegetable System Project of Guizhou (GZCYTX2022-0101); and theConstruction of Guiyang Vegetable Germplasm Resources Research Center (Zhuke contract (2021)No. 5-1).Agronomy 2022, 12, 2582 14 of 18Institutional Review Board Statement: Not applicable.Informed Consent Statement: Not applicable.Data Availability Statement: Not applicable.Conflicts of Interest: The authors declare no conflict of interest.References1. Liang, H.X. On the evolution and distribution in Saururaceae. Acta Bot. Yunnanica 1995, 17, 255–267. (In Chinese with English Titleand Abstract).2. Meng, S.W.; Chen, Z.D.; Li, D.Z.; Liang, H.X. 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Comprehensive Assessment of Houttuynia cordata Thunb., an Important Medicinal Plant and Vegetable
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