Review

Tansley insight
Connecting the pieces: uncovering the
molecular basis for long-distance
communication through plant grafting

Author for correspondence Hannah R. Thomas and Margaret H. Frank

Margaret H. Frank
Tel: +1 607 255 1734 Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA
Email: mhf47@cornell.edu
Received: 28 December 2018
Accepted: 19 February 2019

Contents

Summary 1 V. Interorganismal communication through mobile miRNAs 6

I. Introduction 1 VI. Conclusion 6

II. Defining mobile signals 2 Acknowledgements 7

III. Seasonal changes in development 2 References 7

IV. Systemic signals for drought stress, starvation, and sunlight 4

New Phytologist (2019)
doi: 10.1111/nph.15772
Key words: abiotic responses,
interorganismal communication,
long-distance signaling, plant grafting,
root–shoot communication, sustainable
agriculture.
Summary
Vascular plants are wired with a remarkable long-distance communication system. This network
can span from as little as a few centimeters (or less) in species like Arabidopsis, up to 100 m in the
tallest giant sequoia, linking distant organ systems into a unified, multicellular organism. Grafting
is a fundamental technique that allows researchers to physically break apart and reassemble the
long-distance transport system, enabling the discovery of molecular signals that underlie
intraorganismal communication. In this review, we highlight how plant grafting has facilitated
the discovery of new long-distance signaling molecules that function in coordinating
developmental transitions, abiotic and biotic responses, and cross-species interactions. This
rapidly expanding area of research offers sustainable approaches for improving plant
performance in the laboratory, the field, the orchard, and beyond.

been used to discover mobile proteins, mRNAs, small RNAs, and

I. Introduction
Grafting is an ancient technology that has undergone a modern
renaissance. The first written record of plant grafting dates back to
424 BC (Mudge et al., 2009), and the practice itself probably
originated several millennia before the written record. Grafting is
widely used in agriculture to increase yield, modify branch
architecture, and enhance biotic and abiotic stress tolerance.
Although grafting plays a central role in the successful production
of many crops, the underlying mechanisms that make particular
graft combinations productive remain largely unknown. Indepen-
dent of its application in agriculture, grafting experiments have
small molecules that impact plant morphology (Kim, 2001;
Haywood et al., 2005), reproductive transitions (Corbesier et al.,
2007; Jaeger & Wigge, 2007), host–microbe and plant–parasite
interactions (Shahid et al., 2018; Tsikou et al., 2018), root–shoot
balance (Lin et al., 2014; Spiegelman et al., 2015; Chen et al., 2016;
Landrein et al., 2018), and other fundamental organismal processes
(Martin et al., 2009; Navarro et al., 2011; Takahashi et al., 2018;
Tylewicz et al., 2018). Advances in genomic resources and
molecular techniques that support grafted crops make it possible
for the distinct fields of agricultural and experimental grafting to be
merged. In this review, we highlight newly discovered mobile

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2 Review Tansley insight
signals that have the potential to be translated into agricultural
systems for improved crop resilience.
Reinvigorated interest in plant grafting has led to a recent burst
in publications on the movement and impact of graft-mobile
RNAs, proteins, and small molecules. In some cases, the grafting-
related terminology is ambiguous. In Box 1 and Fig. 1, we define
terminology and illustrate techniques that are commonly used in
plant grafting.
II. Defining mobile signals
Until relatively recently, it was assumed that the majority of RNAs
and proteins are cell-autonomous (i.e. they stay within the cells in
which they are produced), with the exception of a few mobile
molecules that function in intercellular and long-distance com-
munication. However, phloem sap profiling (Buhtz et al., 2008;
Gaupels et al., 2008) and studies using polymorphism-based
detection of mobile mRNAs and small RNAs in heterografted
plants (Yoo et al., 2004; Molnar et al., 2010; Hannapel, 2013;
Thieme et al., 2015; Lewsey et al., 2016; Zhang et al., 2016; Guan
et al., 2017) demonstrate that a large number of RNAs and proteins
are mobile, indicating that not everything that moves necessarily
serves a signaling function. In this review, we refer to graft-mobile
‘signals’ as molecules that are capable of acting at a distance to
influence organismal processes, such as developmental transitions,
morphological responses, nutrient acquisition, and biotic interac-
tions. The extent to which mobile macromolecules function as
signals within the plant communication network (Zhang et al.,
2016) remains an open question (Calderwood et al., 2016; Lee &
Frank, 2018; Morris, 2018). Therefore, we suggest the use of a
separate term, the ‘mobileome’, to discuss the mass collection of
Box 1 Commonly used grafting terminology
‘Grafting’ refers to the physical joining of separate plant parts so that
they share an interconnected vascular system (Melnyk & Meyerow-
itz, 2015). Grafts can be made between any plant parts; however, the
most common graft combination is between ‘stocks’ that comprise
the root system and ‘scions’ that comprise the shoot system.
‘Heterografts’ are formed by grafting distinct genotypes and/or
environmental treatments together (Fig. 1b), whereas ‘homografts’
are formed by grafting together identical genotypes and/or envi-
ronmental treatments (Fig. 1a).
‘Chimera’ is a generic term that refers to an individual composed of
cells that are derived from independent zygotes (Rossant & Spence,
1998). Heterografts are technically chimeras; however, a wide
variety of other cellular arrangements are also defined as chimeras
(Frank & Chitwood, 2016). Therefore, the terms chimera and graft
should not be used interchangeably. One particularly confusing
example of this relates to ‘graft chimeras,’ which consist of cells and
tissues derived from independent genotypes. These plants are
produced by inducing shoot formation along graft junctions, but are
not themselves grafted plants (Tilney-Bassett, 1986). Although each
of these terms sounds similar, they refer to distinct phenomena:
grafting allows researchers to study long-distance signals, whereas
cell-layer chimeras, such as graft chimeras, enable the investigation
of local, cell-to-cell movement.
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RNAs and proteins that have been shown to move, but do not yet
have well-defined functions in long-distance communication.
Future work focused on deciphering the nature and function of
the plant mobileome will help to clarify the degree to which
long-distance macromolecular movement is synonymous with
long-distance signaling (Kehr & Kragler, 2018; Liu & Chen, 2018;
Morris, 2018).
III. Seasonal changes in development
Plants use seasonal cues to align developmental transitions, such as
flowering, bud burst, and the formation of storage organs, with
hospitable environmental conditions (B€aurle & Dean, 2006). The
perception of seasonal information, measured as the photoperiod
(the day : night ratio) in mature leaves, is physically separated from
resulting developmental transitions that typically occur at the apical
ends of plants. This observation led to an initial hypothesis that a
long-distance signaling molecule moves from mature leaves into
the shoot apex to promote flowering (Knott, 1934). To test this
hypothesis, Mikhail Chailakhyan pioneered one of the first grafting
experiments used to track mobile signals; he attached photoperiod-
sensitive short-day scions to long-day stocks and vice versa
(Cha€ılakhyan, 1937). Using these photosensitive heterografts, he
demonstrated that exposure of the stock genotype to inductive
photoperiods (i.e. long-day stocks to long-day light treatments) was
sufficient to trigger reproductive transitions in the scion. These
results formed the basis for Chailakhyan’s ‘florigen’ hypothesis,
stating that a mobile hormone travels through the plant’s long-
distance communication network from mature leaves into the
shoot apex to promote flowering (Cha€ılakhyan, 1937).
It has been nearly a century since the initial demonstration that
florigen functions as a mobile signal (Cha€ılakhyan, 1937), and
nearly two decades since its molecular characterization as
FLOWERING LOCUS T (FT) (Takada & Goto, 2003; An
et al., 2004; Corbesier et al., 2007; Jaeger & Wigge, 2007), and
yet a complete understanding of the mechanisms for florigen
function remain elusive. In addition to traveling as a protein
signal (Corbesier et al., 2007; Jaeger & Wigge, 2007; Mathieu
et al., 2007), there is a substantial body of evidence demonstrat-
ing that FT and related phosphatidylethanolamine-binding
protein (PEPB) family members move as transcripts, some of
which exhibit selective intercellular trafficking (Li et al., 2009,
2011; Jackson & Hong, 2012; Lu et al., 2012; Huang et al.,
2018; Luo et al., 2018). Whether these mobile mRNAs serve as
signals that contribute to the promotion of flowering is a long-
standing point of contention that has been challenging to resolve,
because of the technical difficulty of separating the role of FT
mRNA movement from the demonstrated function of FT protein
in promoting reproductive transitions. Another addition to the
florigen story relates to the spatial regulation of FT, which was
long assumed to be expressed throughout phloem companion
cells. However, recent work shows that FT mRNA expression is
restricted to a previously unidentified, specialized cell type within
the companion cell profile, indicating that FT production is more
spatially refined than once thought, and that morphologically
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(a) Homograft (b) Heterograft (c) Intertaxonomic graft (d) Genetic grafts

Common examples:

Scion

Graft
junction

Stock

Donor Taxon 1 (e.g. eggplant) OE donor WT donor

Recipient Taxon 2 (e.g. tomato) WT recipient Mutant recipient

(e) Transgenic tags (f) Environmental treatment graft

Noninductive Inductive Graft donor Transmit environmental signal
photoperiod photoperiod to recipient (florigen in this example)

Tag donor (e.g. pSUC2:GFP)

Nontransgenic recipient

Fig. 1 Applications of heterografting to uncover mobile molecules. (a) Homografting is performed by physically joining two of the same plants together, and is
commonly used as a control in grafting experiments. (b) Heterografting is a generic grafting technique that involves the physical joining of two or more
independent genotypes (or treatments in the case environmental mobile signals). Specific applications of heterografting are illustrated in (c–f). (c)
Intertaxonomic grafts are heterografts made between independent taxa (e.g. tomato and eggplant); these grafts are frequently used to map the biosynthesis
and mobility of small molecules, proteins and RNAs that differ between grafted species. Intertaxonomic grafting is also used agriculturally to confer beneficial
traits, such as disease-resistant, abiotic stress tolerance and invigorated growth, by combining wild-adapted rootstocks with elite scion cultivars. Note that
mobility can be mapped bidirectionally in intertaxonomic grafts (indicated by the double set of arrows). (d) Genetic grafts are heterografts made between
genetic variants, such as a wild-type donor grafted with a mutant recipient or an overexpression donor grafted with a wild-type recipient. These grafts are
commonly used to test whether a native gene product functions as a long-distance signal. (e) Transgenic tag grafts are used to track protein and RNA mobility
across the graft junction. Green fluorescent protein (GFP) is typically used to visually track proteins, whereas heterologous sequences attached to native
transcripts are used in conjunction with reverse transcription polymerase chain reaction to detect mobile RNAs. This grafting strategy is frequently used to
confirm putative mobile signals that are identified through genetic grafts. (f) Environmental treatment grafts are made between identical genotypes that have
been exposed to independent environmental stimuli, such as noninductive vs inductive photoperiods. Environmental treatment grafts led to the initial discovery
of florigen (Cha€ılakhyan, 1937), and have since been used to uncover a variety of mobile signals that are involved in coordinating organismal responses to the
environment. Blue–orange gradient arrows indicate the directionality of molecular movement from donor to recipient genotypes.

indistinguishable cell types can house distinct molecular func-
tions (Chen et al., 2018).
In addition to controlling flowering time, PEPB family members
regulate a variety of other developmental transitions in a photope-
riod-dependent manner (e.g. tuberization: Martınez-Garcıa et al.,
2002; Navarro et al., 2011; Gonzalez-Schain et al., 2012, and bud
burst:Tylewicz et al., 2018). Work in aspen shows that the breaking
of bud dormancy is controlled through two parallel pathways: an
FT-mediated pathway and an abscisic acid (ABA) mediated
pathway, both of which are photoperiod-dependent. Long days
lead to the increased production of FT1 (an FT ortholog),
promoting the release of bud burst. The expression of FT1 alone.,
however, is insufficient to break bud dormancy. In a second parallel
pathway, short-day winter treatments lead to increased ABA
concentrations, which in turn promote callose synthesis, leading to
the blockage of plasmodesmata (PD) that connect buds to systemic
plant signals. By grafting an ABA synthesis mutant scion, abil1-1,
onto FT1-expressing rootstocks, Tylewicz et al. (2018) demon-
strated that loss of ABA-induced PD closure enables mobile FT1 to
regain entry into buds, inducing bud burst.
Potato tuberization, the differentiation of underground stolons
into vegetative storage organs, is also tightly linked to photoperiod.
Short days induce tuberization, whereas long days inhibit this
developmental transition. Rather than being controlled by a single
mobile signal, grafting experiments from the past two decades show
that photoperiod-dependent induction of tuberization is con-
trolled by multiple, overlapping signals, including mobile proteins
(Navarro et al., 2011; Gonzalez-Schain et al., 2012; Teo et al.,
2016), microRNAs (miRNAs) (Martin et al., 2009; Bhogale et al.,
2013), and mRNAs (Banerjee et al., 2006, 2009). Although it has
long been known that the overexpression and movement of BEL5
transcripts from mature leaves into stolons is sufficient to overcome
the short-day requirement for tuberization (Banerjee et al., 2006,
2009), new work demonstrates that other members of the BEL

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(a)
SAM size
High light

CEP + CEP
receptor Key grafting experiments
HY5
trans- (b) HY5
CEPD Zeatin (shoot to root)
Donor
Scion hy5 HY5–GFP Recipient
hy5 Transgenic tag

Stock HY5–GFP hy5

hy5

(c) CEP peptides (d) CEPD peptides

(root to shoot) (shoot to root)

cepd1/ GFP–
Scion cepr1,2 WT
cepd2 CEPD1

Graft junction GFP– cepd1/

Stock WT cepr1,2
CEPD1 cepd2

High nitrogen HY5 + sucrose Low nitrogen

CEP (e) trans-Zeatin
NO3– (root to shoot)
NRT2.1
NO3– CEPD
– CEPD Scion ipt3.5.7 WT cyp735a1.2 WT
NO3

trans- Stock WT ipt3.5.7 WT cyp735a1.2

Zeatin

Fig. 2 Grafting uncovers a merry-go-round of long-distance signals involved in nitrogen (N) homeostasis. Grafting has facilitated the discovery of long-distance
communication networks that coordinate root–shoot growth responses to N availability (a). Light-responsive ELONGATED HYPOCOTYL 5 (HY5) was shown,
through a series of genetic and transgenic tag grafting experiments (b), to move from shoots to roots. When HY5 is transported into roots, it participates in
sucrose-dependent activation of nitrate transporter, NRT2.1 expression, promoting an increase in N uptake (Chen et al., 2016). An independently discovered
nitrate foraging system balances root growth through a root-to-shoot/shoot-to-root peptide relay. Low-N conditions induce the expression of C-TERMINALLY
ENCODED PEPTIDE (CEP) peptides in roots (a), which were shown to travel into the shoot where they bind CEP receptors (c; highlighted in blue) and trigger the
expression of CEP-DOWNSTREAM (CEPD) response peptides (highlighted in pink) that move back down into the root to induce NRT2.1 expression in a nitrate-
dependent manner (d) (Tabata et al., 2014; Ohkubo et al., 2017). High-nitrate conditions in roots activate the production of trans-Zeatin cytokinin precursors
(highlighted in purple), which were shown, through genetic grafting experiments (e), to move through the xylem into shoots where they participate in the
regulation of shoot apical meristem (SAM) size (Osugi et al., 2017; Landrein et al., 2018). Note that (b–e) illustrate key reciprocal grafting experiments that
were used to demonstrate the movement of long-distance N signals, but are not meant to illustrate all grafting experiments used in the discoveries described.

family also travel as transcripts (Ghate et al., 2017). Surprisingly,
these mRNAs are associated with antituberigen signaling, sup-
pressing rather than promoting tuberization (Ghate et al., 2017).
IV. Systemic signals for drought stress, starvation, and
sunlight
Vascular plants are split between above-ground shoots that
participate in light capture and gas exchange and below-ground
roots that function in nutrient and water foraging. Coordinated
energy allocation between root and shoot growth is essential for
optimizing whole-plant performance. New studies using grafting
have identified signaling molecules that coordinate root–shoot
responses to drought stress (Takahashi et al., 2018), light (Chen
et al., 2016), and nitrogen (N) availability (Tabata et al., 2014;
Chen et al., 2016; Ohkubo et al., 2017; Landrein et al., 2018).
When roots are exposed to water-limiting conditions, there are
rapid physiological responses that protect the plant from desiccation,
including ABA-mediated stomatal closure in the shoot (Roelfsema
et al., 2004). A screen for drought-induced CLAVATA3/EMBRYO
SURROUNDING REGION-RELATED (CLE) peptides in
Arabidopsis roots led to the identification of CLE25, a small,
graft-mobile peptide that moves from roots to shoots (Takahashi
et al., 2018). Grafting experiments demonstrated that wild-type

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Table 1 Movement and function of mobile molecules highlighted in this review.

Phytologist

Mobile molecule Grafting experiment(s) Function Path of movement References

Ó 2019 The Authors

Flowering Locus T
(FT), PEPB, FT1,
protein and
potentially mRNA
Environmental treatment,
confirmed with transgenic tags
and genetic grafting
Promotes flowering, tuberization, and/
or bud burst in response to inductive
photoperiods
From mature leaves into the
meristems of recipient
scions, stolons and/or buds
Cha€ılakhyan (1937); Takada &
Goto (2003); An et al. (2004);
Corbesier et al. (2007); Jaeger
& Wigge (2007); Li et al.
(2009, 2011); Navarro et al.
(2011); Jackson & Hong
(2012); Lu et al. (2012); Huang
et al. (2018); Tylewicz et al.

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(2018)
BELLRINGER1-like 5 Genetic grafting, confirmed Promotes tuberization in response to From leaves to stolons Banerjee et al. (2006, 2009)
(BEL5), mRNA with transgenic tag grafting inductive photoperiods
BEL11 and BEL29, Genetic grafting, confirmed Suppress tuber growth in response to From leaves to stolons Ghate et al. (2017)
mRNAs with transgenic tag grafting photoperiod by repressing target
genes of tuber-promoting BEL1-like
genes
CLE25, small peptide Genetic grafting Promotes rapid drought stress signaling, From root to leaves Takahashi et al. (2018)
by triggering ABA-induced stomatal
closure in leaves
ELONGATED Combination of techniques, Promotes nitrogen uptake and light- From shoot to root Chen et al. (2016)
HYPOCOTYL5 including genetic grafting and dependent carbon/nitrogen
(HY5), protein mobile environmental signal homeostasis
grafting, confirmed with
transgenic tag grafting
C-TERMINALLY Genetic grafting Promote nitrogen foraging From root to shoot Tabata et al. (2014)
ENCODED PEPTIDE
(CEP), small
peptides
CEP DOWNSTREAM Genetic grafting, confirmed Promotes nitrogen uptake by inducing From shoot to root Ohkubo et al. (2017)
(CEPD), small with transgenic tag grafting expression of NRT2.1 nitrate
peptide transporter in roots
Cytokinin precursors, Genetic grafting Promote increased shoot apical From root to shoot apical Osugi et al. (2017); Landrein
small molecules meristem size and growth in response meristem et al. (2018)
to replete nitrogen availability
MicroRNA2111, Genetic grafting Promotes increased nodulation in From shoot to root Tsikou et al. (2018)
small RNA response to low nitrogen
concentrations
Mobile mRNAs Intertaxonomic grafting, Unknown, implicated in systemic Bidirectional movement Hannapel (2013); Thieme et al.
confirmed with transgenic tag nitrogen and phosphate responses from shoot to root and from (2015), Zhang et al. (2016)
grafting root to shoot
Mobile small RNAs Intertaxonomic grafting and Transcriptional gene silencing and post- Predominately from shoot to Yoo et al. (2004), Molnar et al.
Tansley insight

transgenic tag (reporter gene transcriptional gene silencing root, but some movement (2010), Lewsey et al. (2016)
silencing), confirmed with from root to shoot
genetic grafts

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roots are capable of complementing drought-induced responses
in cle25 scions by inducing the expression of NINE-CIS-
EPOXYCAROTENOIDDIOXYGENASE3(NCED3),anessential
enzyme in the ABA biosynthetic pathway in shoots, thus triggering
stomatal closure. However, the extent to which CLE25 serves as a
necessary, endogenous mobile signal during drought responses
remains unclear, as wild-type scions grafted onto cle25 rootstocks
phenocopy wild-type self-grafts (Takahashi et al., 2018).
A balance between whole-plant carbon (C) fixation and N
uptake requires communication between photosynthetic leaves and
N-acquiring roots. In an Arabidopsis mutant screen, elongated
hypocotyl5 (hy5) lines were found to be lacking in shoot-illuminated
root growth (Chen et al., 2016). HY5 is a light-induced transcrip-
tion factor that is necessary for root-induced expression of the high-
affinity nitrate transporter NRT2.1. By grafting mobile and
immobilized versions of HY5-expressing shoots onto hy5 roots,
Chen et al. (2016) showed that shoot-to-root mobility of the HY5
protein is necessary to restore shoot-illuminated root growth via the
direct, sucrose-dependent upregulation of NRT2.1 (Fig. 2a,b).
Taken together, these findings support a role for shoot-mobile HY5
in the homeostatic regulation of C and N balance throughout the
plant (Chen et al., 2016).
Root systems exhibit plasticity in response to heterogeneous
N environments (Ruffel et al., 2011). The transit of small
C-TERMINALLY ENCODED PEPTIDE (CEP) and CEP
DOWNSTREAM (CEPD) peptides from root to shoot and shoot
to root, respectively, serve in the long-distance coordination of this
N-induced plasticity (Fig. 2a,c,d; Tabata et al., 2014; Ohkubo
et al., 2017). Local N starvation in roots induces root-expressed
CEP signals that travel through the xylem into the shoot where they
bind to LRR-RK (Leucine-rich repeat receptor kinase) CEP
receptors (Tabata et al., 2014). In response to CEP perception,
shoot-expressed CEPD peptides move through the phloem into the
root where they selectively activate NRT2.1 expression in nitrate-
rich environments (Ohkubo et al., 2017). Split root nitrate supply
assays demonstrate that local nitrate availability rather than CEPD
trafficking is responsible for selective activation of NRT2.1, which
occurs through an as-yet-unknown mechanism (Ohkubo et al.,
2017).
Recent progress in our understanding of nitrate-induced shoot
plasticity has also been made through grafting. Genetic regula-
tion of shoot apical meristem (SAM) size is relatively well
studied (reviewed in Galli & Gallavotti, 2016); however, the
influence of nutrient availability on SAM size regulation is
poorly understood. Recognizing that well-nourished Arabidopsis
grown with supplemental nitrate exhibits a significantly larger
SAM size and higher growth rate, Landrein et al. (2018) set out
to identify the molecular signals that connect nutrient sensing in
the root with SAM regulation. The researchers identified
mutants that are defective in early steps of cytokinin biosynthesis
(isopentyl transferase3.5.7 and cyp735a1.2) that specifically
desensitize the SAM to increased nitrate availability when they
are grafted as rootstocks, but not as scions, indicating that
cytokinin precursors relay nutrient information regarding nitrate
status from roots to shoots (Landrein et al., 2018) (Fig. 2a,e).
Additional support for a model involving cytokinins as mobile
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root-to-shoot signals comes from previous work showing that
cytokinins synthesized in the root are transported through the
xylem into the shoot, and serve a necessary function in regulating
shoot growth (Osugi et al., 2017).
V. Interorganismal communication through mobile
miRNAs
Plants engage in symbiotic and parasitic interactions through
coordinated interorganismal communication. Two recent studies
used grafting to uncover miRNAs that participate in this commu-
nication system during symbiotic plant–microbe and pathogenic
plant–parasite interactions (Shahid et al., 2018; Tsikou et al.,
2018). Members of the legume family participate in tight symbiotic
associations with N-fixing rhizobia through the formation of
specialized root-derived nodules. Until recently, it was assumed
that nodules were exclusively induced by rhizobial infection. New
work using plant grafting demonstrates that plants maintain
internal regulation over their competency to nodulate through the
shoot-to-root transit of miR2111, which targets and directs post-
transcriptional suppression of TOO MUCH LOVE, a negative
regulator of rhizobial symbiosis (Tsikou et al., 2018).
Plant parasites form ‘haustoria’ with their hosts, through which
xylem and, in a subset of parasites, phloem connections bridge the
two species. In addition to the transfer of nutrients and photosyn-
thates, RNA sequencing of Cuscuta, a parasite that connects to both
xylem and phloem host vascular systems, revealed that thousands of
mRNAs move through the haustorium in a host-to-parasite
direction (Kim et al., 2014). Small RNA sequencing of host–
parasite connections recently demonstrated that genetic material is
bidirectionally transferred across the haustorium, with parasite-
specific miRNAs traveling in reverse, from Cuscuta back into the
host. Several of these Cuscuta miRNAs trigger targeted degradation
of host transcripts that have implicated functions in host defense
(Shahid et al., 2018). Engineering miRNA-resistant transcripts
into economically important plants that are susceptible to Cuscuta
may offer a solution for creating parasite resistant crops.
VI. Conclusion
Long-distance communication serves a pivotal role in vascular plant
success,enablingplantstocoordinatedevelopmentaltransitionswith
seasonal cues, maintain root–shoot balance under fluctuating
environments, and regulate interorganismal interactions. The
technologically simple application of plant grafting has facilitated a
rapid expansion of what was once a short list of known long-distance
signals. These newly discovered signals emanate from diverse classes
of molecules (mRNAs, small RNAs, proteins and small molecules),
providingdeeperinsightinto the molecularinteractionsthat underlie
optimized organismal function (listed in Table 1). Grafting is widely
used in both annual and perennial crop production (Warschefsky
et al., 2016; Gaion et al., 2017). Future work that extends our
knowledge of mobile signals regulating agriculturally relevant traits
(e.g. nutrient foraging, reliable flowering time, symbiotic interac-
tions, and resistance to parasites) into commonly grafted crops
systems offers promising avenues for sustainable crop protection.
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Acknowledgements
We thank two anonymous reviewers for their helpful feedback.
Research in the Frank laboratory is supported through startup
funds from Cornell University’s College of Agriculture and Life
Science. HRT is supported through a graduate student teaching
assistantship from Cornell University.
ORCID
Margaret H. Frank https://orcid.org/0000-0002-8269-8240
Hannah R. Thomas https://orcid.org/0000-0001-5538-2331
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