The Host Stomatal Density Determines Resistance to <i>Septoria gentianae</i> in Japanese Gentian

Tateda, Chika; Obara, Kazue; Abe, Yoshiko; Sekine, Reiko; Nekoduka, Syuuichi; Hikage, Takashi; Nishihara, Masahiro; Sekine, Katsuyuki; Fujisaki, Koki

doi:10.1094/mpmi-05-18-0114-r

Cited by 11 publications

(10 citation statements)

References 65 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Furthermore, disease‐related symptoms in plants with fewer stomata were reduced for several days after inoculation, suggesting that a decrease in pathogen entry points gives the plant additional time to mount an appropriate defence response (Figure ). Our findings are supported by the recent demonstration that reducing SD on the leaves of cultivars of Gentiana trifolia slows the rate of Septoria gentianae fungal infection, with leaves with the highest SD showing the greatest incidence of infection (Tateda et al, ). Our results indicate that plants may actively reduce stomatal development in newly developing leaves as a means to acclimate to bacterial disease pressure.…”

Section: Discussionsupporting

confidence: 88%

Bacterial infection systemically suppresses stomatal density

Dutton

Hõrak

Hepworth

et al. 2019

Plant Cell & Environment

View full text Add to dashboard Cite

Many plant pathogens gain entry to their host via stomata. On sensing attack, plants close these pores to restrict pathogen entry. Here, we show that plants exhibit a second longer term stomatal response to pathogens. Following infection, the subsequent development of leaves is altered via a systemic signal. This reduces the density of stomata formed, thus providing fewer entry points for pathogens on new leaves. Arabidopsis thaliana leaves produced after infection by a bacterial pathogen that infects through the stomata (Pseudomonas syringae) developed larger epidermal pavement cells and stomata and consequently had up to 20% reductions in stomatal density. The bacterial peptide flg22 or the phytohormone salicylic acid induced similar systemic reductions in stomatal density suggesting that they might mediate this effect. In addition, flagellin receptors, salicylic acid accumulation, and the lipid transfer protein AZI1 were all required for this developmental response. Furthermore, manipulation of stomatal density affected the level of bacterial colonization, and plants with reduced stomatal density showed slower disease progression. We propose that following infection, development of new leaves is altered by a signalling pathway with some commonalities to systemic acquired resistance. This acts to reduce the potential for future infection by providing fewer stomatal openings.

show abstract

Section: Discussionsupporting

confidence: 88%

Bacterial infection systemically suppresses stomatal density

Dutton

Hõrak

Hepworth

et al. 2019

Plant Cell & Environment

View full text Add to dashboard Cite

show abstract

“…The model predicts that in most cases, increasing stomatal cover should lead to a proportional increase in colonization, which agrees with empirical studies (e.g., McKown et al, 2014;Dutton et al, 2019;Fetter et al, 2019;Tateda et al, 2019). It also makes new, testable predictions that are less intuitive ( Table 2).…”

Section: Discussionsupporting

confidence: 81%

“…The stomatal and mesophyll conductance to CO 2 are two major limits to photosynthesis (Flexas et al, 2018;Lawson et al, 2018) that are partially determined by stomatal anatomy. Since CO 2 conductance limits photosynthesis (Farquhar and Sharkey, 1982;Jones, 1985) and pathogen infection can reduce fitness (Gilbert, 2002), this sets up a potential tradeoff between increased photosynthesis and defense against pathogens mediated by stomatal anatomy (McKown et al, 2014;Dutton et al, 2019;Fetter et al, 2019;Tateda et al, 2019). For example, plants could increase photosynthetic rate by developing more stomata, but more stomata could result in more pathogen colonization.…”

Section: Introductionmentioning

confidence: 99%

“…In addition to stomatal closure, anatomical changes in stomatal density and/or size might provide another layer of defense against pathogen colonization. For example, infection increases in leaves with higher stomatal density (McKown et al, 2014;Dutton et al, 2019;Fetter et al, 2019;Tateda et al, 2019). The positive effect of stomatal density on infection suggests that infection is limited by the number or size of locations for colonization, meaning that many individual pathogens must usually be unable to find stomata or other suitable locations for colonization.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

Muir

2020

Front. Plant Sci.

View full text Add to dashboard Cite

Stomatal pores control leaf gas exchange and are one route for infection of internal plant tissues by many foliar pathogens, setting up the potential for tradeoffs between photosynthesis and pathogen colonization. Anatomical shifts to lower stomatal density and/or size may also limit pathogen colonization, but such developmental changes could permanently reduce the gas exchange capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen colonization on the leaf as a function of stomatal size and density, anatomical traits which partially determine maximum rates of gas exchange. The model predicts greater stomatal size or density increases the probability of colonization, but the effect is most pronounced when the fraction of leaf surface covered by stomata is low. I also derived scaling relationships between stomatal size and density that preserves a given probability of colonization. These scaling relationships set up a potential anatomical conflict between limiting pathogen colonization and minimizing the fraction of leaf surface covered by stomata. Although a connection between gas exchange and pathogen defense has been suggested empirically, this is the first mathematical model connecting gas exchange and pathogen defense via stomatal anatomy. A limitation of the model is that it does not include variation in innate immunity and stomatal closure in response to pathogens. Nevertheless, the model makes predictions that can be tested with experiments and may explain variation in stomatal size and density among plants. The model is generalizable to many types of pathogens, but lacks significant biological realism that may be needed for precise predictions.

show abstract

“…The stomatal and mesophyll conductance to CO 2 are two major limits to photosynthesis (Lawson et al, 2018; Flexas et al, 2018) that are partially determined by stomatal anatomy. Since CO 2 conductance limits photosynthesis (Farquhar and Sharkey, 1982; Jones, 1985) and pathogen infection can reduce fitness (Gilbert, 2002), this sets up a potential tradeoff between increased photosynthesis and defense against pathogens mediated by stomatal anatomy (McKown et al, 2014; Tateda et al, 2019; Dutton et al, 2019; Fetter et al, 2019). For example, plants could increase photosynthetic rate by developing more stomata, but more stomata could result in more pathogen colonization.…”

Section: Introductionmentioning

confidence: 99%

A stomatal model of anatomical tradeoffs between gas exchange and pathogen colonization

Muir

2019

Preprint

View full text Add to dashboard Cite

2Stomatal pores control both leaf gas exchange and are an entry for many plant pathogens, 3 setting up the potential for tradeoffs between photosynthesis and defense. To prevent colonization 4 and limit infection, plants close their stomata after recognizing pathogens. In addition to closing 5 stomata, anatmoical shifts to lower stomatal density and/or size may also limit pathogen 6 colonization, but such developmental changes would permanently reduce the gas exchange 7 capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen 8 colonization on the leaf as a function of stomatal size and density, anatomical traits which 9 determine maximum rates of gas exchange. The model predicts greater stomatal size or density 10 increases colonization, but the effect is most pronounced when stomatal cover is low. I also 11 derived scaling relationships between stomatal size and density that preserves a given probability 12 of colonization. These scaling relationships set up a potential conflict between maximizing defense 13 and minimizing stomatal cover. To my knowledge, this is the first mathematical model connecting 14 gas exchange and pathogen defense via stomatal anatomy. It makes predictions that can be 15 tested with experiments and may explain variation in stomatal anatomy among plants. The model 16 is generalizable to many types of pathogens, but lacks significant biological realism that may be 17 needed for accurate predictions. 18 19 20 Berry et al., 2010; Chater et al., 2017), but many plant pathogens take advantage of these chinks in the 21 leaf cuticular armor to infect prospective hosts (Zeng et al., 2010; McLachlan et al., 2014; Melotto et al., 22 2017). The density and size of stomata set the anatomical maximum rate of stomatal conductance to CO 2 23 and water vapor (Brown Harrison et al., 2019), but 25 the pore area shrinks and expands in response to internal and external factors to regulate gas exchange 26 dynamically (Buckley, 2019). Many plant pathogens, including viruses (Murray et al., 2016), bacteria 27 ( Melotto et al., 2006; Underwood et al., 2007), protists (Fawke et al., 2015), and fungi (Hoch et al., 1987; 28 Zeng et al., 2010) use stomatal pores to gain entry into the leaf. Since stomatal conductance is a major 29 limitation on photosynthesis (Farquhar and Sharkey, 1982; Jones, 1985) while pathogens reduce fitness, 30 this sets up a potential tradeoff between increased photosynthesis and defense against pathogens. Although 31 there have been many empirical studies on the effect that pathogens have on stomata, there is no theoretical 32 1 Muir et al. Stomata tradeoff photosynthesis for defenseframework in which to place these findings. Lack of a theoreatical framework makes it difficult to answer 33 general questions about how selection for pathogen defense constrains maximum rates of gas exchange. 34Stomatal anatomy is the key link between gas exchange and pathogen colonization. The density and 35 size of stomata not on...

show abstract

The Host Stomatal Density Determines Resistance to Septoria gentianae in Japanese Gentian

Cited by 11 publications

References 65 publications

Bacterial infection systemically suppresses stomatal density

Bacterial infection systemically suppresses stomatal density

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

A stomatal model of anatomical tradeoffs between gas exchange and pathogen colonization

Contact Info

Product

Resources

About