Citation: Barman A, Sahoo L, Ray SK. Some Conspicuous Traits in Domesticated Rice Oryza Sativa, Due To Recessive Alleles. J Plant Sci Res. 2016;3(1): 143.

Introduction

Generally, all observable features in an organism are perceivedas functional gene attributes. However, this is not the case always.Interestingly, there are certain features in organisms that areconsequences of non-functional genes rather than functional ones. Itis difficult to elucidate how non-functional gene contributes toward afeature in an organism. However, there are several examples in naturewhere non-functional alleles confer distinct traits to organisms. Forinstance, several features like fruit shape and size, stature of plants,fragrance of seed etc. established in commonly cultivated plantsare due to occurrence of non-functional or recessive alleles in theirgenomes [1-6]. It is noteworthy that prevalence of these kinds offeatures also has contributed immensely towards their domesticationprocesses [1,7]. The features due to non-functional or recessive alleles follow quantitative mode of inheritance (Figure 1a) and generallydo not comply with the dominant mode of inheritance (Figure 1b).Due to recessive or quantitative pattern of inheritance in these traits,identifying them without specific selection procedures is not easy.

Figure 1: (a): A cross between a tall plant (with 7nos leaves) and a dwarf plant (with 3nos leaves) giving rise to F1 generation plant bearing phenotypic features intermediate between both the parent plant i.e. intermediate height and leaf number(5nos). This inheritance pattern follows quantitative modeand differ from typical Mendelian inheritance trend. Generally, polymorphisms at specific QTLs occurring in the genome account for such phenotypic expressions. (b) A cross between a tall plant (with 7nos leaves) and a dwarf plant (with 3nos leaves) giving rise to F1 generation plant bearing phenotypic features of the tall parent plant (with 7nos leaves) which is the dominant of the two parents. This follows typical Mendelian inheritance pattern.

In domesticated rice (O. sativa), several important traits areknown to be due to recessive or non-functional alleles at specificQTLs [3-14]. To be precise, few conspicuous features of O. sativalike seed fragrance, semi-dwarf stature, resistance to pathogen etc.have established its significance in agronomy. These qualities areresult of mutated or recessive alleles at specific QTLs, coding for nonfunctionalprotein/enzyme. As a matter of fact, presence of recessivealleles in them doesn’t hinder other important characters. Here, wesummarize four important conspicuous traits in O. sativa that allowthem to sustain even in the absence of functional alleles without reduction in their yield.

Rice fragrance

Fragrance is considered an important criterion for determiningquality of a particular cereal and also it is used to comprehend acereal’s endemic identity [2,4]. Basmati rice of India and Jasminerice of Thailand are important because of their distinctive fragrances.Research in this aspect has revealed that fragrance trait in rice is dueto a single gene locus on chromosome 8 called fgr [8,9]. A mutationin wild type BADH2 gene of this locus that code for a betainealdehyde dehydrogenase enzyme results in recessive allele badh2.1.It is believed that the truncated protein product of this recessiveallele is unable to catabolize the oxidation of ϒ-aminobutyraldehydewhich is normally catabolized by intact BADH2 protein [15,16].This defective pathway leads to accumulation of a precursor of thecompound 2-acetyl-1-pyrroline (2AP; Figure 2) and thus enhancedsynthesis of 2AP. The characteristic fragrance in rice is due to thepresence of this compound i.e. 2AP [17,18]. Though there is anotherisoform of betaine aldehyde dehydrogenase gene in rice (denoted asBADH-1 located in chromosome 4), it plays no role in rice fragrance[19]. Furthermore, fragrance due to 2AP resembles that of pandan(Pandanus amaryllifolius L.) and is exhaled by several other plantssuch as cucumber (Cucumis sativus L.), aromatic soybean (Glycinemax (L.) Merr.), aromatic sorghum (Sorghum bicolor (L.) Moench)etc. [6]. It appears that BADH-2 gene and metabolite 2AP has wideincidence amongst different generas of plants despite their differencesat phylogenetic level.

Figure 2: (a): Chemical structure of 2-acetyl-1-pyrroline, redrawn after Buttery et al. [45]. A mutation in wild type BADH2 gene of a single locus on chromosome 8 of rice that code for a truncated protein is unable to catabolize the oxidation of Ï’-aminobutyraldehyde [15,16]. This defect in the pathway lead to accumulation of a precursor of this compound and thus emanating enhanced synthesis of 2AP. The characteristic fragrance in rice is due to the presence of this compound i.e. 2AP [17,18].

Green revolution rice

Green revolution rice refers to semi-dwarf rice variety IR8 thatwas introduced in 1960s as a measure to increased global fooddemand.The characteristic short stature of the rice variety protectsthem from rain and wind, allowing efficient use of nitrogen fertilizersin them and hence contributes to its yield [3,20,21]. Semi-dwarftrait in IR8 is due to mutation in a gene called sd1 (semi dwarf).Basically sd1 comprises of two independent alleles located in thechromosome 1 of rice [22]. Wild type sd1 encodes an oxidase enzymethat metabolizes bio-synthesis of the phyto-hormone gibberellinwhich in turn determines plant height. This particular enzyme namedas GA20 oxidase (GA20ox-2) catalyzes three key conversion stepsi.e. GA53  GA44 GA19  GA20 (Figure 3) during gibberellin biosynthesis process [3]. A removal of 280 bp within the coding regionof this GA20ox-2 gene [22] (results in mutation in the sd1 gene). Thismutation in turn leads to accumulation of GA53 in the plant there byhindering the conversion process. The mutant plant in experimentalconditions was found to be responsive to the externally supplied GA20suggesting that low level of gibberellin is the cause for this heightreduction. In rice, there is another GA oxidase gene coding for GA20ox-1 enzyme that occur in a different chromosome. Though GA20ox-1 and GA20 ox-2 are paralogous but their expression varies indifferent tissues. Therefore, although mutation in GA20 ox-2 affectsplant height but do not hinder grain yield in rice [3].

Figure 3: (One of the pathway showing Gibberellin biosynthesis in which GA 20-oxidase activity is necessary, redrawn after Qiao et al. [46]. Wild type sd1 gene in rice encodes for GA20 oxidase (GA20ox-2) enzyme that metabolizes bio-synthesis of the phyto-hormone gibberellin and this in turn determines plant height. This particular enzyme catalyzes three key conversion stepsi.e. GA53  GA44 GA19  GA20 during gibberellin bio-synthesis process.Mutation in sd1 gene leads to accumulation of GA53 in the plant there byhalting the conversion process and accounts for semi-dwarf feature [3].

Similar to rice, there is also a green revolution dwarf wheat variety.In case of green revolution wheat, dwarfing condition conferringsimilar benefit is due to a mutant allele at one of the Reduced height-1 loci [23]. Here, mutation leads to a gain-of-function transcriptionfactor that makes the plant unresponsive to Gibberellin hormoneand lead to reduced height [23]. The green revolution rice strikinglydiffer from that of the green revolution wheat both at genetic andbiochemical levels. Unlike green revolution rice, dwarfing in wheat is due to a semi-dominant gain-of-function mutation at one of thealleles encoding a DNA binding protein determining height of wheatplant.

Resistance to plant pathogen

Plant resistance to incoming pathogen community is mostlygoverned by gene for gene hypothesis which was proposed by Flor inearly 1940s [24]. According to the hypothesis, resistance in planta isgoverned by presence of R gene (for resistance) in the plant and an avrgene (for avirulence) in the pathogen. Absence of either of the genesor both the genes results in pathogenic condition. The hypothesis isnow a proven fact in many plant-pathogen interactions. The gene forgene hypothesis also predicts resistance as a dominant trait. However,there are evidences of plant-resistance being a recessive trait in several plant-pathogen interactions. The first elucidation of plant-resistance as a recessive trait was in barley which is conferred by an allele called mlo [25]. The molecular characterization of mlo allele suggested that wild type Mlo encodes a component that negatively regulates leaf cell death [26].

Interaction amongst rice and its bacterial pathogen Xanthomonasoryzae pv oryzae (Xoo) also follows the gene for gene hypothesis.Different R genes known in rice are Xa13, Xa17, Xa21, Xa26 etc.[27,28]. Out of these, resistance due to Xa13 and Xa17 are inheritedrecessively. Recent studies have unveiled role of wild type Xa13 intransport of sucrose from phloem parenchyma to apoplast region inrice leaves [29]. After gaining entry inside rice leaves, Xoo upregulates expression of these proteins by manipulating some of its elicitorssecreted via type III protein secretion system. An increased levelof these proteins ensures constant availability of sucrose inside thexylem and permits the pathogen to survive longer. Likewise, Xa17encoded protein also transports sucrose to phloem apoplast. In otherwords, these two genes function paralogously in rice and are namedas sweet proteins. Xoo cause disease in rice by deploying a kind ofeffectors called TALE (transcription activator like effectors) whichin turn upregulates Xa13 synthesis. Rice plant harboring mutatedXa13 will be unresponsive to Xoo TALE effectors and thus resistantto disease condition. Similarly, Xoo TALE effectors are also capable ofup regulating Xa17 synthesis leading to disease symptoms. Althoughit is known that Xoo resides in xylem and is able to deploy its type IIIeffectors for regulating gene expression in phloem parenchyma, themechanism by which the pathogen does it remain to be elucidated.Figure 4b depicts the phenomenon how pathogen entry andinduction leads to expression of sweet transporter proteins evenin mesophyll cells of leaf. Figure 4a shows the usual extracellularsucrose transport mechanism in the absence of pathogen [30].

Figure 4a: Schematic representation of the mechanism of sucrose transport from mesophyll cells to sieve element/companion cells in leaf, redrawn after Chen [30]. Sucrose produced photo-synthetically in the mesophyll cells is translocated within cells through the plasmodesmata and then to the phloem parenchyma cells. From phloem parenchyma cells sucrose is transported to extracellular milieu by SWEET sucrose effluxer, which are thought to bepresent in plasma membrane of the former. Following this, sucrose reachessieve element/companion cells via an ATPase driven H+-coupled sucrosesymporter SUT/SUC [30].

Figure 4b: Schematic representation of the mechanism by which pathogen gain access of sucrose synthesized in the mesophyll cells, redrawn after Chen [30]. Pathogen is able to induce expression of SWEET sucrose effluxers even in the mesophyll cells apart from phloem parenchymatous cells. In this way the pathogen receives nutrition inside the host [30].

In one report corresponding to Xa13, it has been said thatthe former also has a pivotal role in the pollen development indomesticated rice [31]. Mutations in the promoter region ofdominant Xa13 gene lead to down regulated expression that in turncause recessive state of the gene i.e. xa13. This condition leads to malesterility due to hindered pollen development and simultaneouslyconfers race specific resistance to bacterial blight pathogen [31].Presence of paralogs possibly compensate for the mutated dominantgenes.

Considering the important role of sweet transport proteins akinto Xa13 and other proteins in regulating pathogenesis mechanisms,research in this aspect carries lots of promises. Another xylem residentbacterial pathogen, Ralstonia solanacearum has also been shown toderive sucrose from the plant during infection process [32]. Whether recessive trait for sucrose transport function would have similarimpact on R. solanacearum pathogenesis too would be an intriguingquestion in plant-microbe interaction genetics. One stimulatingaspect is regarding the adaptability of both of these xylem pathogens.Xoo is a foliar pathogen, and R. solanacearum invades through rootfirst before spreading to entire plant system through xylem. How,both the pathogens are able to derive sucrose in this environmentmanipulating their type III protein secretion system elicitors will bean interesting comparative study between these two pathogens fortheir pathogenesis in near future.

Non seed-shattering trait in rice

Non-seed shattering trait of O. sativa is an important qualitythat has significantly influenced its domestication processes [33].Anthropogenic selection of the non-seed shattering rice variety overseed-shattering ones has gradually established the former. Geneticbasis of non-seed shattering trait has been connected with a numberof QTLs in rice genome such as sh3, sh4, sh6, sh8, qsh1, qsh2, qsh5,qsh11, qsh12, and sh-h [34-36]. More specifically a QTL sh4 encodesfor a transcription factor with varied functionalities [35b,37]. It hasbeen said that an alteration of a single nucleotide from G to T in thesh4 gene locus results in incomplete development and inadequateabscission zone function leading to non-shattering character of O.sativa [35b]. It is not known, if O. sativa possesses a paralog for thesame gene function in its genome. However, there is no effect on theproductivity of the rice cultivar with this sh4 mutation, similar toother features discussed above. Although, there are different viewswith respect to the significance of sh4 for the non-shattering featurein rice [38], but, recessive state of sh4 carrying this alteration hascertainly been shown to have prominent effect on the non-shatteringtrait of domesticated rice [35b]. Perhaps, with time, more number ofQTLs may be discovered, and it is possible that a cumulative effectof all these QTLs might be necessary for the feature discussed above.